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Microbial life in the phyllosphere

Key Points

  • The surface area of the phyllosphere is approximately twice as great as the land surface area, and this environment provides a habitat for numerous microorganisms that colonize leaf surfaces (where they mostly form aggregates) and the spaces inside leaves.

  • Most phyllosphere microorganisms are bacteria, are non-pathogenic and belong to a few predominant phylogenetic groups, including the classes Alphaproteobacteria and Gammaproteobacteria and the phyla Bacteroidetes and Actinobacteria. The fungi that are also detected in the phyllosphere appear to be hyperdiverse.

  • Numerous biotic and abiotic factors, including the plant itself, drive microbial community structure in the phyllosphere.

  • Targeted and large-scale metaproteogenomic studies have helped to identify important mechanisms by which bacteria adapt to the phyllosphere. These mechanisms include aggregate formation, surface alterations by the production of biosurfactants, the induction of stress responses, and metabolic adaptations ranging from utilization of the C1 compound methanol to utilization of various amino acids and sugars.

  • The phyllosphere is a discrete habitat (or a sum of discrete habitats) and is a tractable model system for understanding the relationships between microorganisms and hosts. An improved understanding of phyllosphere microbiology is also of practical importance for biocontrol of the phyllosphere as the primary carbon-fixing unit in terrestrial systems.

Abstract

Our knowledge of the microbiology of the phyllosphere, or the aerial parts of plants, has historically lagged behind our knowledge of the microbiology of the rhizosphere, or the below-ground habitat of plants, particularly with respect to fundamental questions such as which microorganisms are present and what they do there. In recent years, however, this has begun to change. Cultivation-independent studies have revealed that a few bacterial phyla predominate in the phyllosphere of different plants and that plant factors are involved in shaping these phyllosphere communities, which feature specific adaptations and exhibit multipartite relationships both with host plants and among community members. Insights into the underlying structural principles of indigenous microbial phyllosphere populations will help us to develop a deeper understanding of the phyllosphere microbiota and will have applications in the promotion of plant growth and plant protection.

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Figure 1: The phyllosphere environment.
Figure 2: Microbial phyllosphere diversity.
Figure 3: Bacterial genera detected in the phyllosphere.
Figure 4: Proposed bacterial traits involved in adaptation to the phyllosphere.
Figure 5: Multipartite interactions occur in the phyllosphere among commensal and pathogenic microorganisms and between microorganisms and the plant.

References

  1. Ruinen, J. Occurrence of Beijerinckia species in the phyllosphere. Nature 177, 220–221 (1956).

    Article  Google Scholar 

  2. Woodward, F. I. & Lomas, M. R. Vegetation dynamics – simulating responses to climatic change. Biol. Rev. 79, 643–670 (2004).

    Article  CAS  PubMed  Google Scholar 

  3. Lindow, S. E. & Brandl, M. T. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69, 1875–1883 (2003). An excellent review summarizing earlier work on phyllosphere microbiology.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Baldotto, L. E. B. & Olivares, F. L. Phylloepiphytic interaction between bacteria and different plant species in a tropical agricultural system. Can. J. Microbiol. 54, 918–931 (2008).

    Article  CAS  PubMed  Google Scholar 

  5. Leveau, J. H. J. & Lindow, S. E. Appetite of an epiphyte: quantitative monitoring of bacterial sugar consumption in the phyllosphere. Proc. Natl Acad. Sci. USA 98, 3446–3453 (2001). A seminal paper showing the heterogeneity of available fructose and/or sucrose on leaf surfaces.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Miller, W. G., Brandl, M. T., Quinones, B. & Lindow, S. E. Biological sensor for sucrose availability: relative sensitivities of various reporter genes. Appl. Environ. Microbiol. 67, 1308–1317 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Remus-Emsermann, M. N., Tecon, R., Kowalchuk, G. A. & Leveau, J. H. Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere. ISME J. 6, 756–765 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Boller, T. & Felix, G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379–406 (2009).

    CAS  PubMed  Google Scholar 

  9. Hirano, S. S. & Upper, C. D. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae— a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 64, 624–653 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Wilson, M., Hirano, S. S. & Lindow, S. E. Location and survival of leaf-associated bacteria in relation to pathogenicity and potential for growth within the leaf. Appl. Environ. Microbiol. 65, 1435–1443 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Beattie, G. A. & Lindow, S. E. The secret life of foliar bacterial pathogens on leaves. Annu. Rev. Phytopathol. 33, 145–172 (1995).

    Article  CAS  PubMed  Google Scholar 

  12. Delmotte, N. et al. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl Acad. Sci. USA 106, 16428–16433 (2009). A paper describing the application of a metaproteogenomic approach to the analysis of complex bacterial communities in the phyllosphere of three different model plants. The paper reveals a high consistency among the communities, suggesting that there are unifying adaptive mechanisms among commonly found bacteria.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Whipps, J. M., Hand, P., Pink, D. & Bending, G. D. Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol. 105, 1744–1755 (2008).

    Article  CAS  PubMed  Google Scholar 

  14. Redford, A. J. & Fierer, N. Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb. Ecol. 58, 189–198 (2009).

    Article  PubMed  Google Scholar 

  15. Yang, C. H., Crowley, D. E., Borneman, J. & Keen, N. T. Microbial phyllosphere populations are more complex than previously realized. Proc. Natl Acad. Sci. USA 98, 3889–3894 (2001). The first cultivation-independent study to demonstrate that the diversity of phyllosphere bacteria is complex.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jumpponen, A. & Jones, K. L. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol. 184, 438–448 (2009).

    CAS  PubMed  Google Scholar 

  17. Finkel, O. M., Burch, A. Y., Lindow, S. E., Post, A. F. & Belkin, S. Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl. Environ. Microbiol. 77, 7647–7655 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kim, M. et al. Distinctive phyllosphere bacterial communities in tropical trees. Microb. Ecol. 63, 674–681 (2012).

    Article  PubMed  Google Scholar 

  19. Knief, C. et al. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6, 1378–1390 (2012).

    Article  CAS  PubMed  Google Scholar 

  20. Andrews, J. H., Spear, R. N. & Nordheim, E. V. Population biology of Aureobasidium pullulans on apple leaf surfaces. Can. J. Microbiol. 48, 500–513 (2002).

    Article  CAS  PubMed  Google Scholar 

  21. Morris, C. E., Monier, J. M. & Jacques, M. A. A technique to quantify the population size and composition of the biofilm component in communities of bacteria in the phyllosphere. Appl. Environ. Microbiol. 64, 4789–4795 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Monier, J. M. & Lindow, S. E. Frequency, size, and localization of bacterial aggregates on bean leaf surfaces. Appl. Environ. Microbiol. 70, 346–355 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tecon, R. & Leveau, J. H. The mechanics of bacterial cluster formation on plant leaf surfaces as revealed by bioreporter technology. Environ. Microbiol. 14, 1325–1332 (2012).

    Article  CAS  PubMed  Google Scholar 

  24. Perez-Velazquez, J. et al. Stochastic modeling of Pseudomonas syringae growth in the phyllosphere. Math. Biosci. 239, 106–116 (2012).

    Article  CAS  PubMed  Google Scholar 

  25. Monier, J. M. & Lindow, S. E. Spatial organization of dual-species bacterial aggregates on leaf surfaces. Appl. Environ. Microbiol. 71, 5484–5493 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Rastogi, G. et al. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 6, 1812–1822 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Arnold, A. E. & Lutzoni, F. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88, 541–549 (2007).

    Article  PubMed  Google Scholar 

  28. Lambais, M. R., Crowley, D. E., Cury, J. C., Bull, R. C. & Rodrigues, R. R. Bacterial diversity in tree canopies of the Atlantic forest. Science 312, 1917 (2006).

    Article  CAS  PubMed  Google Scholar 

  29. von Mering, C. et al. Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 315, 1126–1130 (2007).

    Article  CAS  PubMed  Google Scholar 

  30. Stark, M., Berger, S. A., Stamatakis, A. & von Mering, C. MLTreeMap - accurate Maximum Likelihood placement of environmental DNA sequences into taxonomic and functional reference phylogenies. BMC Genomics 11, 461 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Beattie, G. A. & Marcell, L. M. Comparative dynamics of adherent and nonadherent bacterial populations on maize leaves. Phytopathology 92, 1015–1023 (2002).

    Article  PubMed  Google Scholar 

  32. Knief, C., Frances, L. & Vorholt, J. A. Competitiveness of diverse Methylobacterium strains in the phyllosphere of Arabidopsis thaliana and identification of representative models, including M. extorquens PA1. Microb. Ecol. 60, 440–452 (2010).

    Article  PubMed  Google Scholar 

  33. Feil, H. et al. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc. Natl Acad. Sci. USA 102, 11064–11069 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Innerebner, G., Knief, C. & Vorholt, J. A. Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl. Environ. Microbiol. 77, 3202–3210 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. da Silva, A. C. et al. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417, 459–463 (2002).

    Article  PubMed  Google Scholar 

  36. Brandl, M., Clark, E. M. & Lindow, S. E. Characterization of the indole-3 acetic acid (IAA) biosynthetic pathway in an epiphytic strain of Erwinia herbicola and IAA production in vitro. Can. J. Microbiol. 42, 586–592 (1996).

    Article  CAS  Google Scholar 

  37. Vanden Wymelenberg, A., Cullen, D., Spear, R. & Andrews, J. Regulated expression of green fluorescent protein under the control of Aureobasidium pullulans xylanase gene xynA. FEMS Microbiol. Lett. 181, 205–209 (1999).

    Article  CAS  PubMed  Google Scholar 

  38. Knief, C., Ramette, A., Frances, L., Alonso-Blanco, C. & Vorholt, J. A. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J. 4, 719–728 (2010). A comprehensive cultivation-independent study showing the importance of plant species and site for the community composition of ubiquitous methylobacteria.

    Article  CAS  PubMed  Google Scholar 

  39. Kadivar, H. & Stapleton, A. E. Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microb. Ecol. 45, 353–361 (2003).

    Article  CAS  PubMed  Google Scholar 

  40. Yutthammo, C., Thongthammachat, N., Pinphanichakarn, P. & Luepromchai, E. Diversity and activity of PAH-degrading bacteria in the phyllosphere of ornamental plants. Microb. Ecol. 59, 357–368 (2010).

    Article  CAS  PubMed  Google Scholar 

  41. Suda, W., Nagasaki, A. & Shishido, M. Powdery Mildew-infection changes bacterial community composition in the phyllosphere. Microbes Environ. 24, 217–223 (2009).

    Article  PubMed  Google Scholar 

  42. Ikeda, S. et al. Autoregulation of nodulation interferes with impacts of nitrogen fertilization levels on the leaf-associated bacterial community in soybeans. Appl. Environ. Microbiol. 77, 1973–1980 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Zimmerman, N. B. & Vitousek, P. M. Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc. Natl Acad. Sci. USA 109, 13022–13027 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Jumpponen, A. & Jones, K. L. Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol. 186, 496–513 (2010).

    Article  CAS  PubMed  Google Scholar 

  45. Redford, A. J., Bowers, R. M., Knight, R., Linhart, Y. & Fierer, N. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ. Microbiol. 12, 2885–2893 (2010). An article providing evidence that there is a predictable bacterial phyllosphere community pattern which is dependent on the relatedness of trees.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Hunter, P. J., Hand, P., Pink, D., Whipps, J. M. & Bending, G. D. Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca species) phyllosphere. Appl. Environ. Microbiol. 76, 8117–8125 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kniskern, J. M., Traw, M. B. & Bergelson, J. Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol. Plant Microbe Interact. 20, 1512–1522 (2007).

    Article  CAS  PubMed  Google Scholar 

  48. Balint-Kurti, P., Simmons, S. J., Blum, J. E., Ballare, C. L. & Stapleton, A. E. Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol. Plant Microbe Interact. 23, 473–484 (2010).

    Article  CAS  PubMed  Google Scholar 

  49. Cook, R. J. et al. Molecular mechanisms of defense by rhizobacteria against root disease. Proc. Natl Acad. Sci. USA 92, 4197–4201 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100 (2011).

    Article  CAS  PubMed  Google Scholar 

  51. Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95 (2012).

    Article  CAS  PubMed  Google Scholar 

  52. Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Darrasse, A. et al. Transmission of plant-pathogenic bacteria by nonhost seeds without induction of an associated defense reaction at emergence. Appl. Environ. Microbiol. 76, 6787–6796 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Lindow, S. E., Andersen, G. & Beattie, G. A. Characteristics of insertional mutants of Pseudomonas syringae with reduced epiphytic fitness. Appl. Environ. Microbiol. 59, 1593–1601 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Wichmann, G. & Bergelson, J. Effector genes of Xanthomonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genetics 166, 693–706 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lee, J. et al. Type III secretion and effectors shape the survival and growth pattern of Pseudomonas syringae on leaf surfaces. Plant Physiol. 158, 1803–1818 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Melotto, M., Underwood, W., Koczan, J., Nomura, K. & He, S. Y. Plant stomata function in innate immunity against bacterial invasion. Cell 126, 969–980 (2006). A study showing the importance of coronatine produced by P. syringae pv. tomato str. DC3000 for the prevention of MAMP-triggered stomata closing.

    Article  CAS  PubMed  Google Scholar 

  58. Schellenberg, B., Ramel, C. & Dudler, R. Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Mol. Plant Microbe Interact. 23, 1287–1293 (2010).

    Article  CAS  PubMed  Google Scholar 

  59. Jacobs, J. L., Carroll, T. L. & Sundin, G. W. The role of pigmentation, ultraviolet radiation tolerance, and leaf colonization strategies in the epiphytic survival of phyllosphere bacteria. Microb. Ecol. 49, 104–113 (2005).

    Article  CAS  PubMed  Google Scholar 

  60. Gunasekera, T. S. & Sundin, G. W. Role of nucleotide excision repair and photoreactivation in the solar UVB radiation survival of Pseudomonas syringae pv. syringae B728a. J. Appl. Microbiol. 100, 1073–1083 (2006).

    Article  CAS  PubMed  Google Scholar 

  61. Gourion, B., Rossignol, M. & Vorholt, J. A. A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth. Proc. Natl Acad. Sci. USA 103, 13186–13191 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Beattie, G. A. Water relations in the interaction of foliar bacterial pathogens with plants. Annu. Rev. Phytopathol. 49, 533–555 (2011). A review that provides an integrated summary of the various aspects and consequences of water availability for microorganisms in the phyllosphere.

    Article  CAS  PubMed  Google Scholar 

  63. Monier, J. M. & Lindow, S. E. Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Proc. Natl Acad. Sci. USA 100, 15977–15982 (2003). An investigation that uses epifluorescence microscopy to demonstrate that aggregate formation by a phyllosphere bacterium is important for tolerating environmental stresses.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Yu, J., Penaloza-Vazquez, A., Chakrabarty, A. M. & Bender, C. L. Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol. Microbiol. 33, 712–720 (1999).

    Article  CAS  PubMed  Google Scholar 

  65. Chang, W. S. et al. Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J. Bacteriol. 189, 8290–8299 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Rigano, L. A. et al. Biofilm formation, epiphytic fitness, and canker development in Xanthomonas axonopodis pv citri. Mol. Plant Microbe Interact. 20, 1222–1230 (2007).

    Article  CAS  PubMed  Google Scholar 

  67. Bunster, L., Fokkema, N. J. & Schippers, B. Effect of surface-active Pseudomonas spp. on leaf wettability. Appl. Environ. Microbiol. 55, 1340–1345 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Schreiber, L. et al. Plant–microbe interactions: identification of epiphytic bacteria and their ability to alter leaf surface permeability. New Phytol. 166, 589–594 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Axtell, C. A. & Beattie, G. A. Construction and characterization of a proU-gfp transcriptional fusion that measures water availability in a microbial habitat. Appl. Environ. Microbiol. 68, 4604–4612 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Chen, C. & Beattie, G. A. Pseudomonas syringae BetT is a low-affinity choline transporter that is responsible for superior osmoprotection by choline over glycine betaine. J. Bacteriol. 190, 2717–2725 (2008).

    Article  CAS  PubMed  Google Scholar 

  71. Freeman, B. C., Chen, C. L. & Beattie, G. A. Identification of the trehalose biosynthetic loci of Pseudomonas syringae and their contribution to fitness in the phyllosphere. Environ. Microbiol. 12, 1486–1497 (2010).

    CAS  PubMed  Google Scholar 

  72. Wink, M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64, 3–19 (2003).

    Article  CAS  PubMed  Google Scholar 

  73. Giddens, S. R., Houliston, G. J. & Mahanty, H. K. The influence of antibiotic production and pre-emptive colonization on the population dynamics of Pantoea agglomerans (Erwinia herbicola) Eh1087 and Erwinia amylovora in planta. Environ. Microbiol. 5, 1016–1021 (2003).

    Article  CAS  PubMed  Google Scholar 

  74. Stoitsova, S. O., Braun, Y., Ullrich, M. S. & Weingart, H. Characterization of the RND-type multidrug efflux pump MexAB-OprM of the plant pathogen Pseudomonas syringae. Appl. Environ. Microbiol. 74, 3387–3393 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Fan, J. et al. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331, 1185–1188 (2011).

    Article  CAS  PubMed  Google Scholar 

  76. Haefele, D. M. & Lindow, S. E. Flagellar motility confers epiphytic fitness advantages upon Pseudomonas syringae. Appl. Environ. Microbiol. 53, 2528–2533 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Rojas, C. M., Ham, J. H., Deng, W. L., Doyle, J. J. & Collmer, A. HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc. Natl Acad. Sci. USA 99, 13142–13147 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Das, A., Rangaraj, N. & Sonti, R. V. Multiple adhesin-like functions of Xanthomonas oryzae pv. oryzae are involved in promoting leaf attachment, entry, and virulence on rice. Mol. Plant Microbe Interact. 22, 73–85 (2009).

    Article  CAS  PubMed  Google Scholar 

  79. Weibull, J., Ronquist, F. & Brishammar, S. Free amino-acid-composition of leaf exudates and phloem sap: a comparative-study in oats and barley. Plant Physiol. 92, 222–226 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Fiala, V., Glad, C., Martin, M., Jolivet, E. & Derridj, S. Occurrence of soluble carbohydrates on the phylloplane of maize (Zea mays L): variations in relation to leaf heterogeneity and position on the plant. New Phytol. 115, 609–615 (1990).

    Article  CAS  Google Scholar 

  81. Tukey, H. B. Leaching of substances from plants. Annu. Rev. Plant Physiol. 21, 305–324 (1970).

    Article  CAS  Google Scholar 

  82. Remus-Emsermann, M. N. P. & Leveau, J. H. J. Linking environmental heterogeneity and reproductive success at single-cell resolution. ISME J. 4, 215–222 (2010).

    Article  PubMed  Google Scholar 

  83. Brandl, M. T. & Lindow, S. E. Contribution of indole-3-acetic acid production to the epiphytic fitness of Erwinia herbicola. Appl. Environ. Microbiol. 64, 3256–3263 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Limtong, S. & Koowadjanakul, N. Yeasts from phylloplane and their capability to produce indole-3-acetic acid. World J. Microbiol. Biotechnol. 11 Aug 2012 (doi:10.1007/s11274-012-1144-9).

    Article  CAS  PubMed  Google Scholar 

  85. Fry, S. C. Cellulases, hemicelluloses and auxin-stimulated growth: a possible relationship. Physiol. Plant. 75, 532–536 (1989).

    Article  CAS  Google Scholar 

  86. Fall, A. & Benson, A. A. Leaf methanol — the simplest natural product from plants. Trends Plant Sci. 1, 296–301 (1996).

    Article  Google Scholar 

  87. Galbally, I. E. & Kirstine, W. The production of methanol by flowering plants and the global cycle of methanol. J. Atmos. Chem. 43, 195–229 (2002).

    Article  CAS  Google Scholar 

  88. Sy, A., Timmers, A. C. J., Knief, C. & Vorholt, J. A. Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl. Environ. Microbiol. 71, 7245–7252 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Kawaguchi, K., Yurimoto, H., Oku, M. & Sakai, Y. Yeast methylotrophy and autophagy in a methanol-oscillating environment on growing Arabidopsis thaliana leaves. PLoS ONE 6, e25257 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Abanda-Nkpwatt, D., Musch, M., Tschiersch, J., Boettner, M. & Schwab, W. Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J. Exp. Bot. 57, 4025–4032 (2006).

    Article  CAS  PubMed  Google Scholar 

  91. Wellner, S., Lodders, N. & Kampfer, P. Diversity and biogeography of selected phyllosphere bacteria with special emphasis on Methylobacterium spp. Syst. Appl. Microbiol. 34, 621–630 (2011).

    Article  CAS  PubMed  Google Scholar 

  92. Saito, T. & Yokouchi, Y. Stable carbon isotope ratio of methyl chloride emitted from glasshouse-grown tropical plants and its implication for the global methyl chloride budget. Geophys. Res. Lett. 35, L08807 (2008).

    Article  Google Scholar 

  93. Nadalig, T. et al. Detection and isolation of chloromethane-degrading bacteria from the Arabidopsis thaliana phyllosphere, and characterization of chloromethane utilization genes. FEMS Microbiol. Ecol. 77, 438–448 (2011).

    Article  CAS  PubMed  Google Scholar 

  94. Keppler, F., Hamilton, J. T. G., Brass, M. & Rockmann, T. Methane emissions from terrestrial plants under aerobic conditions. Nature 439, 187–191 (2006).

    Article  CAS  PubMed  Google Scholar 

  95. Ji, P. S. & Wilson, M. Assessment of the importance of similarity in carbon source utilization profiles between the biological control agent and the pathogen in biological control of bacterial speck of tomato. Appl. Environ. Microbiol. 68, 4383–4389 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Wilson, M. & Lindow, S. E. Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl. Environ. Microbiol. 60, 4468–4477 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Rico, A. & Preston, G. M. Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol. Plant Microbe Interact. 21, 269–282 (2008).

    Article  CAS  PubMed  Google Scholar 

  98. Blanvillain, S. et al. Plant carbohydrate scavenging through TonB-dependent receptors: a feature shared by phytopathogenic and aquatic bacteria. PLoS ONE 2, e224 (2007). A comprehensive study that puts forward the hypothesis that TonB-dependent receptors are important as transporters for the uptake of various carbohydrates under environmental conditions.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Papen, H., Gessler, A., Zumbusch, E. & Rennenberg, H. Chemolithoautotrophic nitrifiers in the phyllosphere of a spruce ecosystem receiving high atmospheric nitrogen input. Curr. Microbiol. 44, 56–60 (2002).

    Article  CAS  PubMed  Google Scholar 

  100. Furnkranz, M. et al. Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J. 2, 561–570 (2008).

    Article  CAS  PubMed  Google Scholar 

  101. Marco, M. L., Legac, J. & Lindow, S. E. Pseudomonas syringae genes induced during colonization of leaf surfaces. Environ. Microbiol. 7, 1379–1391 (2005).

    Article  CAS  PubMed  Google Scholar 

  102. Wensing, A. et al. Impact of siderophore production by Pseudomonas syringae pv. syringae 22d/93 on epiphytic fitness and biocontrol activity against Pseudomonas syringae pv. glycinea 1a/96. Appl. Environ. Microbiol. 76, 2704–2711 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Joyner, D. C. & Lindow, S. E. Heterogeneity of iron bioavailability on plants assessed with a whole-cell GFP-based bacterial biosensor. Microbiology 146, 2435–2445 (2000).

    Article  CAS  PubMed  Google Scholar 

  104. Karamanoli, K., Bouligaraki, P., Constantinidou, H. I. A. & Lindow, S. E. Polyphenolic compounds on leaves limit iron availability and affect growth of epiphytic bacteria. Ann. Appl. Biol. 159, 99–108 (2011).

    Article  CAS  Google Scholar 

  105. Atamna-Ismaeel, N. et al. Microbial rhodopsins on leaf surfaces of terrestrial plants. Environ. Microbiol. 14, 140–146 (2012).

    Article  CAS  PubMed  Google Scholar 

  106. Atamna-Ismaeel, N. et al. Bacterial anoxygenic photosynthesis on plant leaf surfaces. Environ. Microbiol. Rep. 4, 209–216 (2012).

    Article  CAS  PubMed  Google Scholar 

  107. Kaczmarczyk, A. et al. 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, 6629–6638 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Francez-Charlot, A. et al. Sigma factor mimicry involved in regulation of general stress response. Proc. Natl Acad. Sci. USA 106, 3467–3472 (2009). Together with reference 61, this report describes the discovery of the PhyR–NepR–σEcfG signaling cascade, which is crucial for epiphytic fitness of phyllosphere bacteria and governs the general stress response in alphaproteobacteria.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Hagen, M. J., Stockwell, V. O., Whistler, C. A., Johnson, K. B. & Loper, J. E. Stress tolerance and environmental fitness of Pseudomonas fluorescens A506, which has a mutation in rpoS. Phytopathology 99, 679–688 (2009).

    Article  CAS  PubMed  Google Scholar 

  110. Schenk, A., Weingart, H. & Ullrich, M. S. The alternative sigma factor AlgT, but not alginate synthesis, promotes in planta multiplication of Pseudomonas syringae pv. glycinea. Microbiology 154, 413–421 (2008).

    Article  CAS  PubMed  Google Scholar 

  111. Schirmer, T. & Jenal, U. Structural and mechanistic determinants of c-di-GMP signalling. Nature Rev. Microbiol. 7, 724–735 (2009).

    Article  CAS  Google Scholar 

  112. Ryan, R. P. et al. Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol. Microbiol. 63, 429–442 (2007).

    Article  CAS  PubMed  Google Scholar 

  113. Newell, P. D., Yoshioka, S., Hvorecny, K. L., Monds, R. D. & O'Toole, G. A. Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens Pf0-1. J. Bacteriol. 193, 4685–4698 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Von Bodman, S. B., Bauer, W. D. & Coplin, D. L. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41, 455–482 (2003).

    Article  CAS  PubMed  Google Scholar 

  115. Quinones, B., Dulla, G. & Lindow, S. E. Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol. Plant Microbe Interact. 18, 682–693 (2005).

    Article  CAS  PubMed  Google Scholar 

  116. Quinones, B., Pujol, C. J. & Lindow, S. E. Regulation of AHL production and its contribution to epiphytic fitness in Pseudomonas syringae. Mol. Plant Microbe Interact. 17, 521–531 (2004). References 115 and 116 demonstrate the importance of quorum sensing for the epiphytic fitness of P. syringae.

    Article  CAS  PubMed  Google Scholar 

  117. Redfield, R. J. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365–370 (2002).

    Article  CAS  PubMed  Google Scholar 

  118. Nieto Penalver, C. G. et al. Methylobacterium extorquens AM1 produces a novel type of acyl-homoserine lactone with a double unsaturated side chain under methylotrophic growth conditions. FEBS Lett. 580, 561–567 (2006).

    Article  CAS  PubMed  Google Scholar 

  119. Ryan, R. P. & Dow, J. M. Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol. 19, 145–152 (2011).

    Article  CAS  PubMed  Google Scholar 

  120. Perez, J. L., French, J. V., Summy, K. R., Baines, A. D. & Little, C. R. Fungal phyllosphere communities are altered by indirect interactions among trophic levels. Microb. Ecol. 57, 766–774 (2009).

    Article  PubMed  Google Scholar 

  121. Thrall, P. H., Hochberg, M. E., Burdon, J. J. & Bever, J. D. Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol. Evol. 22, 120–126 (2007).

    Article  PubMed  Google Scholar 

  122. Little, A. E. F., Robinson, C. J., Peterson, S. B., Raffa, K. E. & Handelsman, J. Rules of engagement: interspecies interactions that regulate microbial communities. Annu. Rev. Microbiol. 62, 375–401 (2008).

    Article  CAS  PubMed  Google Scholar 

  123. Hooper, L. V. Do symbiotic bacteria subvert host immunity? Nature Rev. Microbiol. 7, 367–374 (2009).

    Article  CAS  Google Scholar 

  124. Janzen, D. H. in The Biology of Mutualism (ed. D.H. Boucher) 40–99 (Oxford Univ. Press, 1985).

    Google Scholar 

  125. Kurkcuoglu, S., Degenhardt, J., Lensing, J., Al-Masri, A. N. & Gau, A. E. Identification of differentially expressed genes in Malus domestica after application of the non-pathogenic bacterium Pseudomonas fluorescens Bk3 to the phyllosphere. J. Exp. Bot. 58, 733–741 (2007).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  127. Guarner, F. & Malagelada, J. R. Gut flora in health and disease. Lancet 361, 512–519 (2003).

    Article  PubMed  Google Scholar 

  128. Andrews, J. H. Biological control in the phyllosphere. Annu. Rev. Phytopathol. 30, 603–635 (1992).

    Article  CAS  PubMed  Google Scholar 

  129. Vogel, C., Innerebner, G., Zingg, J., Guder, J. & Vorholt, J. A. A forward genetic in planta screen for the identification of plant-protective traits of Sphingomonas sp. Fr1 against Pseudomonas syringae DC3000. Appl. Environ. Microbiol. 78, 5529–5535 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nature Rev. Microbiol. 8, 15–25 (2010).

    Article  CAS  Google Scholar 

  131. McCormack, P. J., Wildman, H. G. & Jeffries, P. Production of antibacterial compounds by phylloplane-inhabiting yeasts and yeastlike fungi. Appl. Environ. Microbiol. 60, 927–931 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Stromberg, K. D., Kinkel, L. L. & Leonard, K. J. Relationship between phyllosphere population sizes of Xanthomonas translucens pv translucens and bacterial leaf streak severity on wheat seedlings. Phytopathology 89, 131–135 (1999).

    Article  CAS  PubMed  Google Scholar 

  133. Rouse, D. I., Nordheim, E. V., Hirano, S. S. & Upper, C. D. A model relating the probability of foliar disease incidence to the population frequencies of bacterial plant pathogens. Phytopathology 75, 505–509 (1985).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  135. Kinkel, L. L. & Lindow, S. E. Invasion and exclusion among coexisting Pseudomonas syringae strains on leaves. Appl. Environ. Microbiol. 59, 3447–3454 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Stockwell, V. O., Johnson, K. B., Sugar, D. & Loper, J. E. Control of fire blight by Pseudomonas fluorescens A506 and Pantoea vagans C9-1 applied as single strains and mixed inocula. Phytopathology 100, 1330–1339 (2010).

    Article  CAS  PubMed  Google Scholar 

  137. Kim, Y. C. et al. The multifactorial basis for plant health promotion by plant-associated bacteria. Appl. Environ. Microbiol. 77, 1548–1555 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Teplitski, M., Warriner, K., Bartz, J. & Schneider, K. R. Untangling metabolic and communication networks: interactions of enterics with phytobacteria and their implications in produce safety. Trends Microbiol. 19, 121–127 (2011).

    Article  CAS  PubMed  Google Scholar 

  139. De Kempeneer, L., Sercu, B., Vanbrabant, W., Van Langenhove, H. & Verstraete, W. Bioaugmentation of the phyllosphere for the removal of toluene from indoor air. Appl. Microbiol. Biotechnol. 64, 284–288 (2004).

    Article  CAS  PubMed  Google Scholar 

  140. Sandhu, A., Halverson, L. J. & Beattie, G. A. Bacterial degradation of airborne phenol in the phyllosphere. Environ. Microbiol. 9, 383–392 (2007).

    Article  CAS  PubMed  Google Scholar 

  141. Leveau, J. H. & Meyer, K. M. Microbiology of the phyllosphere: a playground for testing ecological concepts. Oecologia 168, 621–629 (2012).

    Article  PubMed  Google Scholar 

  142. Dulla, G. & Lindow, S. E. Quorum size of Pseudomonas syringae is small and dictated by water availability on the leaf surface. Proc. Natl Acad. Sci. USA 105, 3082–3087 (2008). An article showing that induction of the quorum sensing system under in situ conditions is dependent on aggregate size.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Newman, K. L., Chatterjee, S., Ho, K. A. & Lindow, S. E. Virulence of plant pathogenic bacteria attenuated by degradation of fatty acid cell-to-cell signaling factors. Mol. Plant Microbe Interact. 21, 326–334 (2008).

    Article  CAS  PubMed  Google Scholar 

  144. Shepherd, R. W. & Lindow, S. E. Two dissimilar N-acyl-homoserine lactone acylases of Pseudomonas syringae influence colony and biofilm morphology. Appl. Environ. Microbiol. 75, 45–53 (2009).

    Article  CAS  PubMed  Google Scholar 

  145. Dulla, G. F. J. & Lindow, S. E. Acyl-homoserine lactone-mediated cross talk among epiphytic bacteria modulates behavior of Pseudomonas syringae on leaves. ISME J. 3, 825–834 (2009).

    Article  CAS  PubMed  Google Scholar 

  146. Morohoshi, T., Someya, N. & Ikeda, T. Novel N-acylhomoserine lactone-degrading bacteria isolated from the leaf surface of Solanum tuberosum and their quorum-quenching properties. Biosci. Biotechnol. Biochem. 73, 2124–2127 (2009).

    Article  CAS  PubMed  Google Scholar 

  147. Boch, J. et al. Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol. Microbiol. 44, 73–88 (2002).

    Article  CAS  PubMed  Google Scholar 

  148. Tamir-Ariel, D., Navon, N. & Burdman, S. Identification of genes in Xanthomonas campestris pv. vesicatoria induced during its interaction with tomato. J. Bacteriol. 189, 6359–6371 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Yang, S. H. et al. Genome-wide identification of plant-upregulated genes of Erwinia chrysanthemi 3937 using a GFP-based IVET leaf array. Mol. Plant Microbe Interact. 17, 999–1008 (2004).

    Article  CAS  PubMed  Google Scholar 

  150. Okinaka, Y., Yang, C. H., Perna, N. T. & Keen, N. T. Microarray profiling of Erwinia chrysanthemi 3937 genes that are regulated during plant infection. Mol. Plant Microbe Interact. 15, 619–629 (2002).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Work in the author's laboratory is supported by research grants from the Swiss National Science Foundation, the Swiss Federal Institute of Technology Zurich (ETH Zurich), the Vontobel Foundation, the Swiss Commission for Technology and Innovation (CTI), the Swiss Initiative in Systems Biology (SystemsX), the European Science Foundation and the European Union's 7th Framework Programme. The author thanks C. Knief, M. Remus-Emsermann and N. Bodenhausen for comments on the manuscript and the anonymous reviewers for helpful suggestions.

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MG-RAST

Glossary

Perennial deciduous plants

Plants that lose their leaves seasonally and live for more than two years.

Epiphytes

Organisms that colonize the surface of plants.

Oligotrophic

Pertaining to the environment: containing very low levels of nutrients.

Stomata

Openings in leaves; these openings control gas exchange (in particular, of oxygen and carbon dioxide) and water transpiration between the plant interior and the environment.

Trichomes

Epidermal outgrowths of plant surfaces, including the leaves. A common type is a hair, which can be branched or unbranched. Glandular trichomes excrete various exudates.

Hydathodes

Water-exuding pores in the epidermis or margin of leaves.

Apoplast

The intercellular space that surrounds plant cells.

Coronatine

A phytotoxin that is produced by several Pseudomonas syringae pathovars. It consists of coronafacic acid (an analogue of methyl jasmonic acid) and coronamic acid (which resembles 1-aminocyclopropane-1-carboxylic acid, a precursor to ethylene), and has been shown to open stomata.

Syringolin A

The major variant of a family of structurally related small cyclic peptides that are secreted by some phytopathogenic bacterial strains. Syringolin A counteracts stomatal closure by inhibiting the proteasome.

Photolyases

Enzymes that are involved in repairing DNA damage caused by ultraviolet light. These flavoproteins reversibly bind to pyrimidine dimers and convert them back to the original bases, a reaction for which visible light is required.

Trehalose

A disaccharide of two glucose units linked by an α,α-1,1-glycosidic bond. This sugar is important for dessication resistance.

Microorganism-associated molecular pattern

A molecular component that is characteristic for a microorganism. Recognition of such a molecule plays a key part in innate immunity.

Bacteriorhodopsins

Retinal-containing transmembrane proteins that act as light-driven proton pumps.

Axenic

Free of contaminating organisms.

Antibiosis

A biological interaction between two species, whereby one species acts antagonistically to the other one, producing a substance that either inhibits growth of the second species or kills it.

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Vorholt, J. Microbial life in the phyllosphere. Nat Rev Microbiol 10, 828–840 (2012). https://doi.org/10.1038/nrmicro2910

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