Phyllosphere

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In ecology, the phyllosphere is the area that the surfaces of leaves and leaf sheaths form as a habitat for other organisms. The phyllosphere represents the largest biological surface on earth and is populated in particular by numerous microorganisms, primarily bacteria , yeasts and filamentous fungi . In adaptation to a nutrient-poor habitat with a special subsoil (water-repellent cuticle of the leaves) and rapidly changing conditions - for example with regard to moisture and radiation - the phyllosphere inhabitants developed a broad spectrum of survival strategies.

The comparatively young field of phyllosphere research also makes use of molecular biological methods to elucidate the so far only rudimentarily known biodiversity and the complex interrelationships that extend to the role of phyllosphere societies in global material cycles . Initially, the main interest was in the investigation of pathogens in plants, but the importance of the numerous phyllosphere inhabitants that have a neutral or even beneficial effect on their base and that can be used, for example, in biological plant protection, has now been recognized .

Terms

Epiphylles (foliicoles) moss in a mountain rainforest

The term “phyllosphere” was coined in the mid-1950s in analogy to the rhizosphere (the area around the plant roots) for the boundary layer between leaf and atmosphere. It is derived from the ancient Greek names φύλλον phyllon 'leaf' and σφαῖρα sphaira 'sphere', 'ball'. The spatial delimitation of the term phyllosphere (in German sometimes also referred to as leaf space) is handled inconsistently in the specialist literature and is sometimes not limited to leaves and leaf sheaths, but also extends to the surfaces of all aboveground plant organs , including buds, flowers, fruits and stems. Sometimes instead of or in addition the term phylloplane used partly synonymously for Phyllosphere, partly in strict restriction to the actual leaf area, while the term "Phyllosphere" depending on the author deeper lying areas such as the substomatären cavity beneath the stomata or the apoplast may include with .

The phyllosphere is usually populated by numerous microorganisms . These organisms are conceptually often assigned to the " epiphytes ". However, since this generally refers to "epiphytes" (and also includes vascular plants , while phyllosphere research concentrates largely on the microorganisms of the immediate leaf surfaces), many authors use the term " epiphylls ", which is more specific for phyllosphere colonists and is also used in this article; The epiphyllic vascular plants, which are particularly present in the tropical mountain rainforest, are usually not counted as part of the phyllosphere, as they themselves are extensive and leave the zone of the immediate leaf surface. Strictly speaking, however, epiphylls are only those organisms that colonize the upper surface of the leaf, whereas those living on the lower surface of the leaf are “hypophylls”. Epi- and hypophylls are also grouped under the generic term “foliicol”, a designation that has at least partially established itself in the specialist literature , especially for organisms that are visible to the naked eye, such as mosses or lichens .

meaning

The habitat ( Habitat ) Phyllosphere constitutes the largest biological surface of the earth. Based on satellite data, the total terrestrial leaf area is estimated to be about 640 million km² to 1 billion km², which corresponds to about 125% to 200% of the total surface of the earth. The phyllosphere thus offers an extensive and richly structured habitat. The predominant colonists are microorganisms, the consideration of which is generally the focus of phyllosphere research. These are in particular bacteria (the number of which by far dominates), followed by yeasts , filamentous (thread-like) fungi and possibly other groups of organisms: plant viruses , archaea , oomycetes , myxomycetes , green algae , mosses , lichens , ferns , unicellular animals and invertebrates .

Conservative estimates assume a total number of bacteria in the phyllosphere of 10 26 . A plant leaf typically carries one million to 10 million bacteria per square centimeter. Some groups of plants, such as citrus species or conifers , on the other hand, are significantly less populated, sometimes with fewer than 1,000 cells per cm².

Due to its large area, the phyllosphere represents an important refuge and at the same time an important resource for microorganisms. Since these absorb organic matter and later release it again in a modified form, the phyllosphere is also in - in addition to the exchange of substances with the environment via the leaf anyway biogeochemical material cycles are integrated. The number of microorganisms inhabiting the phyllosphere is large enough to be able to influence the global carbon and nitrogen cycles.

While the exploration of the rhizosphere can look back on a longer tradition, the properties, biodiversity and interactions of the phyllosphere inhabitants with the animate and inanimate surroundings have only received increased attention for a few decades. Initially, for economic reasons, the main interest of phyllosphere microbiology was the investigation of pathogens ( pathogens ) in plants in order to understand the mechanisms of their settlement, spread and harmful effects and to be able to take appropriate countermeasures. In the meantime, the important role of the numerous phyllosphere organisms that have a neutral or even beneficial effect on their base has been recognized. The importance of phyllosphere research is taken into account through regular specialist events, including an international phyllosphere symposium, which has been held every 5 years since the first event of this kind in Newcastle upon Tyne in 1970 . The 9th International Symposium on the Microbiology of Aerial Plant Surfaces was hosted by Oregon State University in August 2010 .

Investigation methods

The basis for research into the communities of the phyllosphere, which are often invisible to the naked eye, is the development of suitable research methods. More in-depth insights into complete species spectra are now made possible by modern methods of molecular biology .

Classic procedures

One of the classic methods of investigation for microorganisms in the phyllosphere is what is known as " leaf printing ". A leaf is carefully pressed onto a nutrient medium, such as an agar plate , and then pulled off again. After incubation , the bacterial or fungal colonies that have grown in the meantime are examined. A similar method is the “ leaf washing ” technique : Here, leaves are rinsed in a vessel with a liquid ( e.g. saline solution or phosphate buffer ) and the microorganisms washed off the cuticle are then further cultivated, e.g. by plating on a nutrient medium. Both methods then use light , fluorescence or electron microscopy in combination with microbiological or biochemical methods in order to be able to analyze the grown organisms more precisely. The culture media can contain certain nutrients or inhibiting substances with which different groups of organisms can be distinguished.

However, it should be noted that only some of the epiphyllic microorganisms can be cultivated or form colonies under laboratory conditions. Therefore, with the methods mentioned, only a part of the actually existing spectrum of species can be recorded. They also only depict the microbial population at a specific point in time; Numerous leaf analyzes are required over the entire development period in order to be able to record the changes that are often significant in the course of leaf development.

Molecular biological processes

In addition to morphological or physiological examination methods, methods are now also available with which samples washed off leaves can be examined for the entire genetic material ( genome , in this case the metagenome ) of the organisms obtained. The polymerase chain reaction (PCR) is often used here , with which genetic material is duplicated, in order to then separate it using gel electrophoresis and examine it for certain markers . Such markers form in particular the genes coding for parts of ribosomes (16S rRNA in prokaryotes such as bacteria, 18S rRNA in eukaryotes such as fungi). Similar methods have recently also been used with regard to the totality of proteins ( metaproteome ) using mass spectrometric methods.

Other methods of examination of the habitat phyllosphere are based on the inoculation of leaf surfaces in the laboratory or field with suspensions , the defined bacteria or fungal spores include (single species or strains or mixtures thereof). The subject of research is then in particular their growth success under different environmental conditions and interactions with existing colonists. Genetically modified bacteria are often used as so-called bioreporters or biosensors . These have special reporter genes , often a fluorescent gene (for example, from the luminous jellyfish Aequorea victoria -derived GFP gene) whose activity can be detected readily. With the help of such bioreporters, for example, the presence and distribution of certain substances on leaves, such as nutrients such as various sugars, trace elements or even water, can be detected.

Habitat

Leaf of the nasturtium ( Tropaeolum majus ) with a water-repellent (hydrophobic) cuticle

particularities

The phyllosphere habitat poses particular challenges for the genotypic and phenotypic flexibility of potential colonists, because the leaf surface is a highly uneven habitat. Structurally and functionally distinct regions of the sheet as stomata (stomata), leaf veins , hairs ( trichomes ) and epidermal cells do not only offer a different "topography", but also vary considerably in terms of water retention, thickness of the cuticle or permeability to be herbal substances. The cuticle of the leaves is usually the substrate with which the organisms of the phyllosphere first come into contact or which is colonized by them. It is an extracellular lipophilic biopolymer and mainly consists of cutin in which waxes of various compositions are incorporated or deposited. Their structure shows an often highly complex three-dimensional and crystalloid structure, which can be subject to strong changes in the course of leaf development and often erodes in older leaves.

Guttation on strawberry leaves

In addition to the structural peculiarities of the base, the phyllosphere habitat is characterized by other special physical-chemical conditions. Frequent and rapid changes in the available humidity are characteristic. This is particularly provided by rain, fog or dew and also depends to a large extent on leaf surface structures and their wettability . Other factors that are often characterized by rapid fluctuations are radiation (especially UV light), temperature conditions, wind and the availability of nutrients. This is where the phyllosphere differs from the rhizosphere , for which largely constant or slowly changing conditions are typical. Overall, there is a low supply of water and nutrients in the phyllosphere; only a small part of the nutrients and water transported in the leaf escape to the outside. For example, the guttation fluid of some plant species, which also contains nutrients, can be used for microorganisms . However, the phyllosphere nutrients available to colonists mostly come only to a small extent from the leaf itself, since the cuticula represents a barrier for polar molecules such as sugar or amino acids , but mainly from the atmosphere (nitrogenous compounds, pollen ) or as honeydew from insects . In many cases, the primary limitation of growth for microorganisms is the availability of carbon compounds , and only secondarily the availability of nitrogen .

Settlement strategies

The colonization of the phyllosphere occurs in particular through rain, wind movement (possibly over hundreds of kilometers) or insects. However, the distribution of microorganisms on leaves is very inhomogeneous. Leaf veins, leaf undersides or shaded, base-near areas of glandular hairs or stomata usually show a denser microbial colonization than other leaf zones. The mobility of some microorganisms is advantageous, as it allows them to actively move to suitable locations. In addition to passive adhesion , active mechanisms also come into play for attachment to the hydrophobic leaf surface . For example, attachment can occur through extracellular, water-insoluble glycoproteins or polysaccharides . Some bacteria have special formations for this purpose, such as thin, thread-like protein appendages or tubes ( pili ) or microfibrils made of cellulose . Microorganisms often form larger colonies or aggregates on leaves. A number of species are able to develop so-called biofilms . Biofilms are thin slimy layers that represent a complex matrix of extracellular polysaccharides and other biopolymers and are known from a large number of habitats. They offer the organisms often embedded in large numbers - often a broad spectrum of bacteria, yeasts and filamentous fungi - a more favorable environment, for example in terms of pH value or ionic strength , and provide overall protection against dehydration and environmental influences.

Some species are capable of releasing surface-active substances which, as so-called biosurfactants, reduce the surface tension . This improves the wettability of the hydrophobic leaf surfaces with water and thus increases its availability for microorganisms. An example of an effective biosurfactant is the syringomycin produced by Pseudomonas syringae .

Depending on the rapidly changing environmental conditions, the population density of the phyllosphere is subject to strong temporal fluctuations. Precipitation not only leads to colonization, but also to leaching of existing leaf colonies. Heavy precipitation can therefore lead to significant changes in the population density and structure, but in turn favor repopulation through at least temporary humidification. The time of arrival is also important for potential settlers: first-time settlers usually find more nutrients than later arrivals and face less competition . Organisms that have special adaptation mechanisms at their disposal in order to withstand rapid changes in the environment by means of tolerance or avoidance strategies have survival advantages in the phyllosphere. In addition to creating their own environment through biofilms (see above), many microorganisms in the phyllosphere are able to produce shielding pigments (usually pink, orange or yellow) that protect them from UV radiation. Since radiation brings with it an increased risk of mutation , efficient DNA repair systems can additionally or alternatively be advantageous. Such mechanisms responding to UV-B radiation are known from Pseudomonas syringae , for example .

The ability to colonize deeper areas of the leaf and other plant organs is mainly limited to pathogens. Many fungi are able to penetrate the cuticle by hyphae , which not only allows them to be mechanically fastened, but often also to tap nutrients directly from the leaf. Due to their way of life, they form the transition to endophytism , which, however, is often not clearly distinguishable from epiphytism and the purely epiphyllic way of life and in individual species can also be dependent on environmental conditions or stage of development. A methodological distinction is usually made in that a surface sterilization is survived or not. However, pathogenicity is not necessarily linked to an endophytic way of life.

Species composition and succession

In addition to the population density, the species composition of phyllosphere communities is not static, but characterized by high dynamics, whereby, in addition to environmental factors such as weather or radiation, air pollution can also play a role. Because of the high heterogeneity of the phyllosphere, attempts are being made to transfer biogeographical models of island biogeography to the microscale of the phyllosphere and thus to explain the microbial settlement structure, which sometimes strongly diverges between neighboring leaves.

Bacteria, yeast and fungi

Cultures of Pseudomonas syringae
Cell thread from Anabaena sp.

In temperate latitudes, a chronological sequence ( succession ) of several groups of epiphyllic microorganisms can often be observed in the course of the vegetation period : On young, unfolding leaves, bacteria usually dominate - when the nutrient supply is initially rather low. The species that can easily be cultivated under laboratory conditions often include representatives of oxygen-breathing ( aerobic ) groups of the genera Pseudomonas , including Pseudomonas syringae (one of the best-studied organisms of the phyllosphere), Corynebacterium , Erwinia , Bacillus and Xanthomonas . Likewise frequent, but more difficult to detect in the laboratory because of their slower growth and more specific requirements, are facultative methylotrophic bacteria from the genus Methylobacterium (that is, able to use methanol as a carbon and energy source) . Furthermore, cyanobacteria from the genera Anabaena , Nostoc , Scytonema and Aulosira can live on leaves . If the metagenome is analyzed, there are often still unknown species in the samples, which show that there are still considerable gaps in knowledge of the bacterial epiphylls. For example, 78 types of bacteria from 37 known and 12 previously nameless genera were detected on sugar beet leaves alone .

If more nutrients become available in the course of leaf development (for example in the form of pollen, dust or excrement of leaf-dwelling arthropods, especially sugary honeydew ), yeasts come to the fore. Commonly represented genera are Cryptococcus , Sporobolomyces , Rhodotorula , Torulopsis and Aureobasidium . Species of the genus Sporobolomyces are particularly successful colonizers of the phyllosphere among yeasts, as they can spread efficiently from one leaf to another with the help of so-called ballistospores.

As the leaves age ( senescence ) in autumn, the phyllosphere community is increasingly shaped by filamentous fungi. They originate from the groups of Ascomycota (Ascomycota), Stand mushrooms (Basidiomycota), and the artificial group of imperfect fungi contains the types of unknown systematic arrangement. The genera Epicoccum , Alternaria and Stemphylium , including leaf-damaging species, have been proven . Existing honeydew also forms the nutritional basis for mainly saprophytic , i.e. species that live on dead organic material, such as the so-called sooty fungi . As the leaf senescence continues, almost only saprophytes appear, for example representatives from the genera Ascochytula , Leptosphaeria , Pleospora and Phoma . Allochthonous (that is, from other habitats, especially the soil), the genera Cryptococcus (see above), Myrothecium and Pilobolus are also represented in the phyllosphere along with numerous others. An inventory of the leaves of Mediterranean plants revealed 1029 filamentous fungi and 540 yeast strains, which could be assigned to 36 or 46 different species. As with bacteria, not all species of fungi and yeast are known by far.

Other groups of organisms

The conditions in the subtropical and tropical regions, especially the tropical rainforests with year-round high temperatures and the corresponding humidity (as well as the fact that many plants in the tropics have perennial foliage) allow other groups of species to colonize leaf areas in addition to microorganisms. These include epiphyllic (foliicole) lichens , of which over 800 species are known, 616 alone for the Neotropis , including, for example, representatives of the genera Arthonia , Bacidia , Byssoloma , Mazosia , Porina , Strigula and Tricharia . Among the also very species-rich foliicolen mosses dominate foliose liverworts family Lejeuneaceae ; As early as 1996, around 1,000 liverwort species with an epiphyllic way of life were known, including species from the genera Cololejeunea , Ceratolejeunea , Drepanolejeunea and Colura . There have also been isolated observations of liverworts on long-lived leaves from oceanic climates at higher latitudes, such as ivy ( Hedera helix ) in southern England. If the cuticle degrades with increasing leaf age and the wettability with water increases, green algae will also find suitable conditions. In temperate climates, this applies in particular to the perennial needles of conifers , which are often colonized by representatives of the genus Chlorococcus from the second year onwards.

It has only been known since the late 1990s that the phyllosphere in tropical regions - only exceptionally in a temperate climate - also represents a habitat for the organism group of slime molds (myxomycetes). While mosses and lichens mostly settle on the upper side of the leaves, the slime molds with their various development stages prefer areas that are less exposed to rain or light, i.e. the underside of the leaves or secondary microhabitats formed by epiphyllic liverworts .

Animal unicellular organisms , which are known to feed on bacteria in the soil and water, have often been found on leaves. One example is the hayfish ( Colpoda cucullus ), which has the ability to form cysts when dehydrated so that it can quickly become active again when humidified. The common invertebrate inhabitants of the phyllosphere include nematodes . At least major parts of their lives hold numerous species from other animal groups in the Phyllosphere on, including water bears , annelid worms , snails , mites , diplura , springtails , dust lice , aphids , butterflies and Hymenoptera , especially ants .

Interactions

Inside the phyllosphere

Interactions between the organisms of the phyllosphere take place on the one hand between the colonists and on the other hand between the colonists and their host base, i.e. the leaf. The phyllosphere favors gene exchange through the close aggregation of the microorganisms that colonize it . For example, high rates of horizontal gene transfer have also been demonstrated across species boundaries through the transfer of bacterial plasmids , which probably makes the phyllosphere an important source or hotspot of microbial biodiversity . There are also interactions between different epiphyllene groups that go beyond mere competition, for example leaf-damaging fungi can themselves be colonized by bacteria, ie, parasitized by them, for example Neurospora crassa by Pseudomonas syringae .

The organisms of the phyllosphere can exert neutral influences as commensals , negative influences as pathogens or positive influences as symbionts on their base. There are various ways in which epiphylls can influence a leaf to your advantage and thereby damage it to a greater or lesser extent. The influence can be about in the delivery of plant hormones ( phytohormones ), toxins ( toxins ) or substances consist which the permeability ( permeability increase) of cell membranes, so as to increase the nutrient availability from the sheet. Positive effects (mutualism) for the host plant can result, for example, if its leaves are colonized by nitrogen fixators, their growth is increased by phytohormones of the epiphylls or their presence leads to the suppression of other organisms with pathogenic effects. In many cases, it is not possible to clearly assign the organisms, since environmental factors and the development cycle, especially in the case of bacterial species, determine whether they have a neutral or phytopathogenic effect.

The leaf colonists visible to the naked eye - such as mosses, lichens or green algae - are usually not directly harmful to colonized leaves, but can reduce their photosynthesis performance as the degree of coverage increases . Parasitism is not common among these groups, but it does occur. Examples are green algae of the genus Cephaleuros and lichens of the genus Strigula , in which Cephaleuros species are symbiotic partners .

Powdery mildew on field maple leaf

For a long time, research attention has focused on the numerous phytopathogenic organisms of the phyllosphere. In addition to leaf destroyers such as the many mildew- causing fungi or fire blight pathogens ( Erwinia ), some Erwinia or Pseudomonas species can also promote frost damage through the formation of ice. Leaves often contain biological antifreeze substances that prevent freezing even at temperatures well below 0 ° C. Bacteria that contain the so-called ice gene, such as various strains ( pathovars ) of Pseudomonas syringae , reduce the freezing tolerance of leaves, so that cell-destroying ice crystal formation occurs prematurely. In order to counteract this harmful effect, the first field trials with genetically modified bacteria were carried out, as it was possible to prove that bacterial strains without the ice gene can successfully compete with strains that are harmful to plants. Corresponding bacterial strains are now being sold commercially.

Apple tree infested with fire blight

In order to combat the fire blight pathogen Erwinia amylovora , which is economically very important in fruit growing, non-chemical, competition-based strategies have also been developed in the sense of biological plant protection, which are based on the fact that an early application of antagonistic microorganisms can successfully suppress a later colonization with Erwinia . In general, the positive economic effects of some microorganisms in the form of so-called biological control agents (BCA) for controlling or preventing plant diseases are of growing interest. These are able to control or reduce pathogen infestation on leaf surfaces. Here different mechanisms come into question as competition for nutrients occupation of ecological niches or active inhibition of other types of administration of substances such as acids, cell-res acting enzymes or antibiotic or antifungal acting substances.

Phytohormones of the auxin group are widespread among the bacteria of the phyllosphere and can be effective in many areas of plant development. They can promote plant growth in a positive sense, which also applies to the phytohormone group of cytokinins , which are produced by some Methylobacterium species. Disadvantages for the host arise when phytohormones trigger hyperplasias or leaf deformations or plant galls. Released hormone substances from the phyllosphere inhabitants can also stimulate the release of nutrients from the leaf to the outside, for example via the formation of new ion channels in cell membranes, resulting in an increased outflow of metabolic products. Indole-3-acetic acid (IAA, the most important auxin representative) stimulates the release of saccharides from plant cell walls. In extreme cases, the effects of released substances through epiphylls can lead to the disintegration ( lysis ) of leaf cells.

The leaves of many carrier plants in tropical regions are known to be regularly colonized by nitrogen-fixing ( diazotrophic ) microorganisms. Part of the fixed nitrogen can also be taken up by the host plants in the leaf and used. In particular, diazotrophic cyanobacteria play a key role, which in turn often have a close, sometimes symbiotic bond with epiphyllic mosses. It is believed that such communities make a significant contribution to nitrogen input in tropical rainforests. For a premontaneous rainforest in Costa Rica, nitrogen fixation rates in the phyllosphere of 2 to 5 kg per hectare and year are given (mainly caused by representatives of the genus Scytonema ). The actual capacity of the phyllosphere to fix nitrogen and its importance in the global nitrogen cycle is, however, only insufficiently known.

With people and atmosphere

On the one hand, toxins produced by fungi ( mycotoxins ), which are mostly produced by endophytes, are of direct importance for human nutrition . More recently observed cases of food poisoning, on the other hand, show the risk that ripening fruits or leaf areas of vegetables can be colonized with human pathogenic enterobacteria , such as Salmonella or Shigella , even before harvest (for example through sprinkling with untreated water or fertilizer). Contrary to previous opinion, such bacteria can not only survive but also multiply on such surfaces, especially in humid conditions. Overall, however, little research has been done on the biology of enterobacteria on plant surfaces.

Since surfaces generally represent an important sink for reactive trace gases in the atmosphere, the phyllosphere also plays a not insignificant role in regulating and removing air pollutants such as ozone , sulfur dioxide , ammonia and others. In principle, the complex leaf structures with their wax layers and large surfaces offer a wide range of deposit options for fine particles (dust) or aerosols . The extent to which interactions with the microorganisms of the phyllosphere are of importance in addition to the only partially understood physico-chemical effects on leaf surfaces has hardly been researched. It is known that phyllosphere societies are sensitive to air pollutants such as sulfur dioxide or nitrogen oxides . On the other hand, the presence of heavy metal-resistant bacteria in the phyllosphere can also serve as a positive bio-indicator for certain air pollutants.

literature

  • Bailey MJ, Lilley AK, et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , 315 pp.
  • Steven E. Lindow, Eva I. Hecht-Poinar, Vern J. Elliot (Eds.): Phyllosphere microbiology . APS Press, St. Paul, Minn., 2002, ISBN 978-0-89054-286-6 , 395 pp.
  • Steven E. Lindow, Maria T. Brandl: Microbiology of the phyllosphere . Applied and Environmental Microbiology 69, 2003, pp. 1875-1883, online

Web links

Wiktionary: Phyllosphere  - explanations of meanings, word origins, synonyms, translations

Individual evidence

  1. ↑ FT Last: Seasonal incidence of Sporobolomyces on cereal leaves. Transactions of the British Mycological Society 38, 1955, pp. 221-239.
  2. ↑ Jakoba ruins: Occurrence of "Beijerinckia" species in the phyllosphere . Nature 177, 1956, pp. 220-221.
  3. ^ Wilhelm Gemoll : Greek-German school and hand dictionary. Munich / Vienna 1965.
  4. ↑ Elmar Weiler, Lutz Nover: General and molecular botany . G. Thieme, Stuttgart 2008, ISBN 978-3131476616 , p. 805.
  5. ↑ TM Timms-Wilson, K. Smalla et al .: Microbial Diversity in the Phyllosphere and Rhizosphere of Field Grown Crop Plants: Microbial Specialization at the Plant Surface . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 21-36.
  6. ^ Á Fonseca, J. Inácio: Phylloplane Yeasts . In: C. Rosa and G. Peter (Eds.): Biodiversity and Ecophysiology of Yeasts . Springer, Berlin / Heidelberg 2006, ISBN 978-3540261001 , pp. 263-302.
  7. ↑ a b c Nathanaël Delmotte, Claudia Knief et al .: Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proceedings of the National Academy of Sciences 38, 2009, pp. 16428-16433, online
  8. ↑ a b c d e f g h Steven E. Lindow, Maria T. Brandl: Microbiology of the phyllosphere . Applied and Environmental Microbiology 69, 2003, pp. 1875-1883, online
  9. ^ Rainer Nowak, Sieghard Winkler: Foliicole lichen of the Sierra Nevada de Santa Marta (Colombia) and their mutual relationships. Austrian Botanical Journal 118, 1970, pp. 456-485.
  10. ^ A b Robert Lücking: Foliicolous lichenized fungi . Flora Neotropica Monograph 103. The New York Botanical Garden Press, New York 2008, ISBN 978-0-89327-491-7 , 866 pp.
  11. ^ CE Morris, LL Kinkel: Fifty years of phyllosphere microbiology: Significant contributions to research in related fields. In: Steven E. Lindow, Eva I. Hecht-Poinar, Vern J. Elliot (eds.): Phyllosphere microbiology . APS Press, St. Paul, Minn., 2002, ISBN 978-0-89054-286-6 , pp. 365-375.
  12. ↑ a b c Markus Riederer, Caroline Müller (Ed.): Biology of the plant cuticle . Blackwell Pub., Oxford 2006, ISBN 978-1405132688 , pp. 334-341.
  13. ^ Wilhelm Barthlott, Christoph Neinhuis et al .: Classification and terminology of plant epicuticular waxes . Botanical Journal of the Linnean Society 126 (3), 1998, pp. 237-260.
  14. ↑ J.-F. Monier: Bacterial Assemblages on Plant Surfaces . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 83-105.
  15. ↑ ML Hutchison, MA Tester, DC Gross: Role of biosurfactant and ion channel-forming activities of syringomycin in transmembrane ion flux: a model for the mechanism of action in the plant-pathogen interaction . Molecular Plant-Microbe Interactions 8, 1995, pp. 610-620.
  16. ↑ JJ Kim, GW Sundin: Regulation of the rulAB Mutagenic DNA Repair Operon of Pseudomonas syringae by UV-B (290 to 320 nanometers) Radiation and Analysis of rulAB-Mediated Mutability In Vitro and In Planta . Journal of Bacteriology 182 (21), 2000, pp. 6137-6144, PMID 11029435 , PMC 94749 (free full text).
  17. ↑ P. Bayman: Diversity, Scale and Variation of Endophytic Fungi in Leaves of Tropical Plants . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 37-50.
  18. ↑ RWS Weber, H. Anke: Effects of Endophytes on Colonization by Leaf Surface Microbiota . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 209-222.
  19. ^ A b Steven E. Lindow: Phyllosphere Microbiology: A Perspective . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 1-20.
  20. ↑ SS Hirano, CD Upper: Bacteria in the Leaf Ecosystem with Emphasis on Pseudomonas syringae - a Pathogen, Ice Nucleus, and Epiphyte . Microbiology and Molecular Biology Reviews 64 (3), 2000, pp. 624-653, online
  21. ↑ a b c P. K. Mohapatra: Textbook of Environmental Microbiology . IK International Publishing House Pvt. Ltd., New Delhi 2008, ISBN 978-8190656672 , p. 183.
  22. ↑ Ian P. Thompson, Mark J. Bailey et al .: Short-term community dynamics in the phyllosphere microbiology of field-grown sugar beet. FEMS Microbiology Ecology 16, 2005, pp. 205-211.
  23. ↑ J. Inácio, P. Pereira et al .: Estimation and diversity of phylloplane mycobiota on selected plants in a Mediterranean-type ecosystem in Portugal . Microbial Ecology 44 (4), 2002, pp. 344-353.
  24. ↑ Robert Lücking, Marcela Cáceres: Folicolous lichens of the world , web version (PDF; 2.8 MB)
  25. ↑ Tamás Pócs: Epiphyllous liverwort diversity at worldwide level and its threat and conservation. Anales del Instituto de Biologia, Universidad Nacional Autonoma de Mexico, Botanica series, 67 (1), 1996, pp. 109–127, online (PDF; 1.1 MB)
  26. ^ Jeff Duckett: Epiphyllic and epifungal liverworts on Hampstead Heath, London. Field Bryology 95, 2008, pp. 8–10 online (PDF; 166 kB)
  27. ↑ Markus Riederer, Caroline Müller (ed.): Biology of the plant cuticle. Blackwell Pub., Oxford 2006, ISBN 978-1405132688 , p. 105.
  28. ↑ Uno H. Eliasson: Myxomycetes on living leaves in the tropical rainforest of Ecuador; an investigation based on the herbarium of higher plants. In: Stapfia. Volume 73, Linz 2000, pp. 81-84, PDF on ZOBODAT
  29. ↑ Martin Schnittler: Foliicolous liverworts as a microhabitat for Neotropical Myxomycetes. Nova Hedwigia 72 (1–2), 2001, pp. 259–270, online ( memento of the original from May 10, 2015 in the Internet Archive ) Info: The archive link was inserted automatically and has not yet been checked. Please check the original and archive link according to the instructions and then remove this notice. (PDF; 107 kB) @1@ 2Template: Webachiv / IABot / www.db-thueringen.de
  30. ↑ Robert Lücking, Andrea Bernecker-Lücking: Lichen feeders and lichenicolous fungi: do they affect dispersal and diversity in tropical foliicolous lichen communities? Ecotropica 6, 2000, pp. 23-41.
  31. ↑ a b B. J. Jacobsen: Biological Control of Plant Diseases by Phyllosphere Applied Biological Control Agents . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 131-147.
  32. ↑ TS Schubert: Strigula fries, the union plans parasitic. Plant Pathology Circular 227, 1981, 2 p., Online ( Memento of the original dated December 3, 2010 in the Internet Archive ) Info: The archive link has been inserted automatically and has not yet been checked. Please check the original and archive link according to the instructions and then remove this notice. (PDF; 131 kB) @1@ 2Template: Webachiv / IABot / www.doacs.state.fl.us
  33. ↑ MA Holland, RLG Long, JC Polacco: Methylobacterium spp .: phylloplane bacteria involved in cross-talk with the plant host? In: Steven E. Lindow, Eva I. Hecht-Poinar, Vern J. Elliot (eds.): Phyllosphere microbiology . APS Press, St. Paul, Minn., 2002, ISBN 978-0-89054-286-6 , pp. 125-135.
  34. ↑ Elke Freiberg: Microclimatic parameters influencing nitrogen fixation in the phyllosphere in a Costa Rican premontane rain forest. Oecologia 17, 1998, pp. 9-18
  35. ↑ Michel Fürnkranz, Wolfgang Wanek et al .: Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica . The ISME Journal 2, 2008, pp. 561-570, online
  36. ^ Maria T. Brandl: Human Pathogens and the Health Threat of the Phyllosphere . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 269-285.
  37. ↑ T. Müller, K. Strobel, A. Ulrich: Microorganisms in the Phyllosphere of Temperate Forest Ecosystems in a Changing Environment . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 51-65.
  38. ↑ D. Fowler, JN Cape et al .: Atmospheric Composition and the Phyllosphere: the Role of Foliar Surfaces in Regulating Biogeochemical Cycles . In: MJ Bailey, AK Lilley et al. (Ed.): Microbial Ecology of Aerial Plant Surfaces . CAB International, Wallingford / Oxfordshire 2006, ISBN 978-1845930615 , pp. 305-315.
  39. ^ Franco Baldi, Maria A. Bianco, Milva Pepi: Mercury, arsenic and boron resistant bacteria isolated from the phyllosphere as positive bioindicators of airborne pollution near geothermal plants. In: Science of the Total Environment , 164 (2), 1995, pp. 99-107, doi : 10.1016 / 0048-9697 (95) 04426-2 .
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