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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.

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.

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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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