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.
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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Ruinen, J. Occurrence of Beijerinckia species in the phyllosphere. Nature 177, 220–221 (1956).
Woodward, F. I. & Lomas, M. R. Vegetation dynamics – simulating responses to climatic change. Biol. Rev. 79, 643–670 (2004).
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.
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).
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.
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).
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).
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).
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).
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).
Beattie, G. A. & Lindow, S. E. The secret life of foliar bacterial pathogens on leaves. Annu. Rev. Phytopathol. 33, 145–172 (1995).
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.
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).
Redford, A. J. & Fierer, N. Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb. Ecol. 58, 189–198 (2009).
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.
Jumpponen, A. & Jones, K. L. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol. 184, 438–448 (2009).
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).
Kim, M. et al. Distinctive phyllosphere bacterial communities in tropical trees. Microb. Ecol. 63, 674–681 (2012).
Knief, C. et al. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6, 1378–1390 (2012).
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).
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).
Monier, J. M. & Lindow, S. E. Frequency, size, and localization of bacterial aggregates on bean leaf surfaces. Appl. Environ. Microbiol. 70, 346–355 (2004).
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).
Perez-Velazquez, J. et al. Stochastic modeling of Pseudomonas syringae growth in the phyllosphere. Math. Biosci. 239, 106–116 (2012).
Monier, J. M. & Lindow, S. E. Spatial organization of dual-species bacterial aggregates on leaf surfaces. Appl. Environ. Microbiol. 71, 5484–5493 (2005).
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).
Arnold, A. E. & Lutzoni, F. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88, 541–549 (2007).
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).
von Mering, C. et al. Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 315, 1126–1130 (2007).
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).
Beattie, G. A. & Marcell, L. M. Comparative dynamics of adherent and nonadherent bacterial populations on maize leaves. Phytopathology 92, 1015–1023 (2002).
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).
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).
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).
da Silva, A. C. et al. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417, 459–463 (2002).
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).
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).
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.
Kadivar, H. & Stapleton, A. E. Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microb. Ecol. 45, 353–361 (2003).
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).
Suda, W., Nagasaki, A. & Shishido, M. Powdery Mildew-infection changes bacterial community composition in the phyllosphere. Microbes Environ. 24, 217–223 (2009).
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).
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).
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).
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.
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).
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).
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).
Cook, R. J. et al. Molecular mechanisms of defense by rhizobacteria against root disease. Proc. Natl Acad. Sci. USA 92, 4197–4201 (1995).
Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100 (2011).
Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95 (2012).
Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90 (2012).
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).
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).
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).
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).
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.
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).
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).
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).
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).
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.
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.
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).
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).
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).
Bunster, L., Fokkema, N. J. & Schippers, B. Effect of surface-active Pseudomonas spp. on leaf wettability. Appl. Environ. Microbiol. 55, 1340–1345 (1989).
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).
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).
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).
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).
Wink, M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64, 3–19 (2003).
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).
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).
Fan, J. et al. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331, 1185–1188 (2011).
Haefele, D. M. & Lindow, S. E. Flagellar motility confers epiphytic fitness advantages upon Pseudomonas syringae. Appl. Environ. Microbiol. 53, 2528–2533 (1987).
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).
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).
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).
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).
Tukey, H. B. Leaching of substances from plants. Annu. Rev. Plant Physiol. 21, 305–324 (1970).
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).
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).
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).
Fry, S. C. Cellulases, hemicelluloses and auxin-stimulated growth: a possible relationship. Physiol. Plant. 75, 532–536 (1989).
Fall, A. & Benson, A. A. Leaf methanol — the simplest natural product from plants. Trends Plant Sci. 1, 296–301 (1996).
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).
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).
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).
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).
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).
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).
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).
Keppler, F., Hamilton, J. T. G., Brass, M. & Rockmann, T. Methane emissions from terrestrial plants under aerobic conditions. Nature 439, 187–191 (2006).
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).
Wilson, M. & Lindow, S. E. Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl. Environ. Microbiol. 60, 4468–4477 (1994).
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).
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.
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).
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).
Marco, M. L., Legac, J. & Lindow, S. E. Pseudomonas syringae genes induced during colonization of leaf surfaces. Environ. Microbiol. 7, 1379–1391 (2005).
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).
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).
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).
Atamna-Ismaeel, N. et al. Microbial rhodopsins on leaf surfaces of terrestrial plants. Environ. Microbiol. 14, 140–146 (2012).
Atamna-Ismaeel, N. et al. Bacterial anoxygenic photosynthesis on plant leaf surfaces. Environ. Microbiol. Rep. 4, 209–216 (2012).
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).
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.
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).
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).
Schirmer, T. & Jenal, U. Structural and mechanistic determinants of c-di-GMP signalling. Nature Rev. Microbiol. 7, 724–735 (2009).
Ryan, R. P. et al. Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol. Microbiol. 63, 429–442 (2007).
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).
Von Bodman, S. B., Bauer, W. D. & Coplin, D. L. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41, 455–482 (2003).
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).
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.
Redfield, R. J. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365–370 (2002).
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).
Ryan, R. P. & Dow, J. M. Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol. 19, 145–152 (2011).
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).
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).
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).
Hooper, L. V. Do symbiotic bacteria subvert host immunity? Nature Rev. Microbiol. 7, 367–374 (2009).
Janzen, D. H. in The Biology of Mutualism (ed. D.H. Boucher) 40–99 (Oxford Univ. Press, 1985).
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).
Haas, D. & Defago, G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Rev. Microbiol. 3, 307–319 (2005).
Guarner, F. & Malagelada, J. R. Gut flora in health and disease. Lancet 361, 512–519 (2003).
Andrews, J. H. Biological control in the phyllosphere. Annu. Rev. Phytopathol. 30, 603–635 (1992).
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).
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).
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).
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).
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).
Zamioudis, C. & Pieterse, C. M. J. Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact. 25, 139–150 (2012).
Kinkel, L. L. & Lindow, S. E. Invasion and exclusion among coexisting Pseudomonas syringae strains on leaves. Appl. Environ. Microbiol. 59, 3447–3454 (1993).
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).
Kim, Y. C. et al. The multifactorial basis for plant health promotion by plant-associated bacteria. Appl. Environ. Microbiol. 77, 1548–1555 (2011).
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).
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).
Sandhu, A., Halverson, L. J. & Beattie, G. A. Bacterial degradation of airborne phenol in the phyllosphere. Environ. Microbiol. 9, 383–392 (2007).
Leveau, J. H. & Meyer, K. M. Microbiology of the phyllosphere: a playground for testing ecological concepts. Oecologia 168, 621–629 (2012).
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.
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).
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).
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).
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).
Boch, J. et al. Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol. Microbiol. 44, 73–88 (2002).
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).
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).
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).
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.
The author declares no competing financial interests.
- Perennial deciduous plants
Plants that lose their leaves seasonally and live for more than two years.
Organisms that colonize the surface of plants.
Pertaining to the environment: containing very low levels of nutrients.
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.
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.
Water-exuding pores in the epidermis or margin of leaves.
The intercellular space that surrounds plant cells.
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.
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.
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.
Retinal-containing transmembrane proteins that act as light-driven proton pumps.
Free of contaminating organisms.
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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