Next Article in Journal / Special Issue
Performance and Hydroponic Tomato Crop Quality Characteristics in a Novel Greenhouse Using Dye-Sensitized Solar Cell Technology for Covering Material
Previous Article in Journal
A Dwarf Phenotype Identified in Breadfruit (Artocarpus altilis) Plants Growing on Marang (A. odoratissimus) Rootstocks
Previous Article in Special Issue
Use of Diatomaceous Earth as a Silica Supplement on Potted Ornamentals
Article Menu
Issue 2 (June) cover image

Export Article

Horticulturae 2019, 5(2), 41;

Light and Microbial Lifestyle: The Impact of Light Quality on Plant–Microbe Interactions in Horticultural Production Systems—A Review
Department of Biosystems and Technology, Microbial Horticulture Unit, Swedish University of Agricultural Sciences, SLU, P.O. Box 103, SE-230 53 Alnarp, Sweden
Département de Phytologie, Centre de Recherche et d’Innovation sur les Végétaux (CRIV), Université Laval, Pavillon Envirotron, Local 1216, Québec City, QC G1V 0A6, Canada
Department of Biosystems and Technology, Horticultural Crop Physiology Unit, Swedish University of Agricultural Sciences, SLU, P.O. Box 103, SE-230 53 Alnarp, Sweden
Author to whom correspondence should be addressed.
Received: 15 January 2019 / Accepted: 23 May 2019 / Published: 28 May 2019


Horticultural greenhouse production in circumpolar regions (>60° N latitude), but also at lower latitudes, is dependent on artificial assimilation lighting to improve plant performance and the profitability of ornamental crops, and to secure production of greenhouse vegetables and berries all year round. In order to reduce energy consumption and energy costs, alternative technologies for lighting have been introduced, including light-emitting diodes (LED). This technology is also well-established within urban farming, especially plant factories. Different light technologies influence biotic and abiotic conditions in the plant environment. This review focuses on the impact of light quality on plant–microbe interactions, especially non-phototrophic organisms. Bacterial and fungal pathogens, biocontrol agents, and the phyllobiome are considered. Relevant molecular mechanisms regulating light-quality-related processes in bacteria are described and knowledge gaps are discussed with reference to ecological theories.
abiotic factors; biocontrol agent (BCA); controlled environment; ecological theory; greenhouse; molecular mechanisms; non-phototrophic bacteria; pathogens; phyllosphere; plant metabolism; plant morphology

1. Introduction

Plants are meta-organisms colonized with microorganisms, including bacteria, fungi, algae, archaea, protozoa, viruses, and, on rare occasions, nematodes. Depending on the environmental and plant-related conditions prevailing in the various habitats surrounding different plant organs (e.g., soil/growing medium, atmosphere), different compartments (so-called spheres) differing in microbial colonization patterns and community structure have been identified. The very well-researched zone affected by the root (rhizosphere) consists of an outer layer (ectorhizosphere), the root surface (rhizoplane), and the interior of the root (endorhizosphere). Likewise, aboveground plant parts constitute three spheres, the phyllosphere, caulosphere, and carposphere, which denote zones affected by the leaf, stem, and fruit, respectively. The phyllosphere is divided into the epiphytically colonized leaf surface and the leaf endosphere.
The phyllosphere and its microbiota have received increasing attention during recent years [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33], because this can be a powerful tool to improve plant health, growth, development, and human health metabolites. Studies have been conducted on a wide range of scales, from parts of a leaf to intact leaves, entire canopies of individual plants, and crop stands. Studies on plant stands tend to use the term phyllosphere in a wider sense, including also the caulosphere and carposphere. The phyllosphere can be divided into the epiphytically colonized leaf surface and the leaf endosphere. The leaf surface is a hostile environment for microbes due to exposure to diurnally and seasonally fluctuating environmental and plant physiological conditions and their interactions (e.g., ambient temperature, irradiation, and water and nutrient availability) [30,34,35]. In contrast, the leaf endosphere offers a nutritionally rich and shielded environment [35]. Plant leaves host 106–107 bacteria/cm2 leaf surface [30], with microbially available nutrients (organic carbon sources) being the driving force. However, nutrients are not evenly distributed on the leaf surface, so leaves are not covered with an even biofilm, but rather with patches containing assemblages of microorganisms [17,30,35,36,37]. While the leaf microbiota is affected by external conditions in the habitat, it is also able to respond proactively to suboptimal conditions through the use of light receptor proteins and to modify its habitat to shield itself from harmful environmental effects and to optimize nutrient acquisition and chances of survival [30,35].
Controlled environments, such as greenhouses, polytunnels, and plant factories, reduce the amplitude of fluctuations in the crop environment, which in turn affects plant performance and the structure and function of the associated microbiome. Greenhouse-covering materials and shade netting alter prevailing environmental conditions (e.g., temperature, relative humidity, and carbon dioxide (CO2) concentration), but also conditions at the crop level and in the crop phyllosphere, as they influence greenhouse light transmission, reflection, absorption, and diffusion within the canopy [38,39,40]. Figure 1 summarizes the most important growth parameters affecting the phyllosphere of greenhouse crops.
To compensate for light deprivation under naturally low light conditions and to optimize plant development and quality with respect to crop and market demands, additional artificial assimilation lighting is necessary. Different types of lamps are available (Table 1). Alternative technologies, among these light-emitting diodes (LED), have been introduced during recent years as a measure to reduce energy consumption and costs.
In the horticultural and controlled environment context, light and plant interactions, including light intensity, light quality (light spectrum), and day length, have been well-researched (Figure S2), but studies in these disciplines only rarely consider the fact that plants are meta-organisms. In plant microbiology studies, on the other hand, there has been an increasing focus on the phyllosphere in recent years. Prompted by advances in culture-independent techniques, many of these studies focus on the community structure and microbial biodiversity on a descriptive level, but rarely include ecological theories or concepts [19]. Although such studies are often carried out under controlled climate conditions, description and monitoring of environmental factors receive little attention (Figure S3). In fact, the leaf surface and the phyllosphere are often considered a matrix with limited interactions, rather than part of a living and aging system, and very few studies explicitly consider the impact of light quality on the phyllosphere microbiota under greenhouse conditions. With respect to artificial assimilation lighting, the architecture of the plant and crop stand and the position of the light source (top and/or intracanopy lighting) are important. With a rosette-like leaf organization, all leaves are fully exposed to the administered light, whereas only the most outer leaf layer of cushion-forming plants and plants within dense crop stands is exposed, irrespective of top or intercrop irradiation. Leaves inside the canopy are shaded and, thus, dominated by green light (wavelength: 500–565 nm).
The bacterial community structure in the phyllosphere has received more attention than the fungal community structure. Examples of the bacterial community structure of various greenhouse-grown crops are shown in Figure 2. With respect to foliar pathogens, the focus in previous research has been on alternative control of fungi using different wavelengths of light (light qualities), rather than on bacteria [46,47,48,49,50]. However, different light technologies influence biotic and abiotic conditions in the plant environment [51]. Modifications in the cropping environment, induced by light intensity and quality and by daylength, influence the structure but also the function of the leaf-associated microbiome [51,52,53]. Microbes switch lifestyle to adapt to light qualities, as a matter of life and death (i.e., to enable metabolism, function, survival, growth, and nutrient acquisition) [50,52,53].
In this review, we consider the impact of light quality on plant–microbe interactions in light of current ecological theories and concepts. In particular, we focus on the following research questions:
Which light-dependent plant processes and mechanisms are decisive for phyllosphere colonizers?
Which morphological plant characteristics are modified by light quality and consequently influence the structure and/or function of the phyllosphere microbiome?
Which light-quality-dependent microbial processes and mechanisms affect plant traits?
Which ecological principles and theories apply to microbiome effects in the phyllosphere with regard to artificial illumination?

2. Materials and Methods

In this literature review, we followed recommendations developed for systematic reviews and meta-analyses [54] and covered the literature in a 30-year period (1988–2018). All keywords and keyword combinations are listed in Table S1. Searches were performed in Web of Knowledge (WoK) using all WoK databases (Web of Science Core Collection, Biosis Citation Index, CABI, Current Contents Connect, Data Citation Index, Derwent Innovation Index, KCI-Korean Journal Database, MEDLINE, Russian Science Citation Index, SciELO Citation Index, Zoological Record).

3. Abiotic Effects of Light on the Leaf Microbiota

3.1. Impact of Lighting Technology on Leaf Temperature, Leaf Moisture, and Humidity

The light environment affects the environment of the leaf surface in several ways. In greenhouse conditions, the most profound effect on the leaf microbiota caused by artificial lighting is due to changes in leaf microclimate [55]. Differences in the amount of infrared (IR) light emitted by different types of light sources is the major cause of these light-source-dependent changes in the leaf microclimate [55]. Conventional high-intensity discharge (HID) lamps, including metal halide (MH) and high-pressure sodium (HPS) lamps, emit most of their waste heat as IR radiation, radiated in the same direction as visible light [55]. In contrast, LED-based light sources mainly produce sensible heat, which has to be cooled away from the fixture using fans, heat sinks, or water cooling [55]. It is well-documented that lighting using HID lamps results in higher leaf temperatures than lighting using LED lamps, e.g., one study [56] reported 0.5–0.7 °C higher air temperature in the canopy in plants illuminated with HPS lights compared with plants illuminated with LED lights [56]. Another study found that air temperatures were around 1 °C higher within the crop stand of potted ornamentals when HPS lighting was applied, compared with LED lighting [57]. Moreover, the relative humidity (RH) in the canopy has been found to be around 5%-units lower when HPS lights are applied compared with LED lights [57]. Interactions between UV radiation and relative humidity have also been observed [58]. It was observed that attacks of powdery mildew in roses can be reduced to practically zero when applying 24-h lighting, which has been explained by constant moisture conditions on the leaves preventing conidia from germinating [59]. On the other hand, higher relative humidity (lower vapor pressure deficit) is generally known to increase the incidence of infection and sporulation of Botrytis cinerea [60]. The ambient air temperature also affects the incidence of Botrytis infection in tomato, with an optimum at 15 °C [60].
A number of studies have also demonstrated lower leaf temperatures when using LEDs instead of HPS lamps [58]. Leaf temperatures exceeding the ambient air temperature create air movement within the canopy, thus removing humidity from the boundary layer of the leaf and supplying CO2 to the boundary layer. Leaf temperatures higher than the ambient air temperature also eliminate the risk of condensation on the leaf surfaces at dew point temperatures close to the ambient air temperature.
When producing plants in closed environments (i.e., plant factories), high leaf temperatures can be a problem [61]. However, in greenhouse production, leaf temperatures during winter are often sub-optimal due to losses of radiant heat through the greenhouse roof. The need for supplementary lighting typically arises during periods of the year where the greenhouse also needs supplementary heating due to low outdoor temperatures. In addition, increased light intensities should typically be accompanied by higher ambient temperatures [62].

3.2. Effects of Ultraviolet (UV) Light

The amount of ultraviolet (UV) light emitted by light fixtures affects the conditions for microbial growth on leaf surfaces. Greenhouse-covering materials normally filter out a large proportion of the UV light, making the greenhouse a UV-deficient environment. In particular, conventional glass panes filter out most UV light, whereas some plastic films have good transmittance of both UV-A and, in some cases, UV-B light [63,64,65]. Conventional greenhouse HID fixtures normally emit negligible amounts of UV light, but it is possible to supply UV light by using UV lamps [48].

3.3. Effects of Far Red (FR) Light

At the other end of the light spectrum, far-red (FR) light (710–850 nm) and particularly the red-to-far-red ratio (R:FR photoequilibrium) of light perceived by phytochromes can strongly affect the conditions for the leaf microbiota via physiological processes affecting plant architectural development, flowering, photosynthesis, plant nutrition, and plant tolerance to biotic and abiotic stresses [58,66]. The R:FR ratio varies within the day (e.g., from 0.6 at the beginning and end of the day to 1.0–1.3 at noon) and it is strongly reduced within the canopy (e.g., to 0.03). Greenhouse-covering materials, such as FR-absorbing plastic film, also impact R:FR ratio (e.g., increasing it from 1.0 under natural light up to 5.7) and plant development [67,68].
The spectral distribution of the light also has direct effects on photosynthesis and, thereby, the availability to microbes of carbon sources within the leaf and on the leaf surface. The blue and red parts of the spectrum are generally considered more efficient for photosynthesis than the yellow and green parts [69]. However, more recent research suggests that green light with its better penetration contributes significantly to photosynthesis in the deeper layers of the canopy [70]. Using light sources emitting just red and blue light is, therefore, not recommended [71,72].

4. Plant-Mediated Effects of Light on the Leaf Microbiota

Light is one of the most important environmental factors affecting plant growth, development, and metabolite content. Light within a broad spectrum range (400–700 nm) is essential for plant photosynthesis, plant growth, and crop productivity, while specific light spectra trigger different intracellular processes via diverse photoreceptors that modify gene expression, metabolism, plant morphology, and functions [58,73,74,75]. Figure 3 summarizes plant processes affected by light that can be targeted to promote beneficial phyllosphere components, contributing to greenhouse crop productivity and plant resilience to abiotic and biotic stresses. Modifications in plant architecture, plant morphology, and plant physiology processes will then directly or indirectly impact the leaf microclimate, such as leaf moisture and temperature, as well as habitat resource availability (e.g., carbon, nitrogen, and phosphorus compounds) for the phyllosphere microbiota. However, plant–light interactions are often plant-species-dependent.

4.1. Plant–Light Interactions

4.1.1. Plant Architecture and Leaf Morphology

Modulation of light spectra (e.g., R:FR ratio) to control plant architecture and leaf morphology is a well-known technique used by producers of ornamental plants to improve the shape and appearance of their plants, while assimilation lighting (400–700 nm) of vegetables improves crop productivity. However, both these artificial lighting regimens modify the canopy microclimate and plant structure. Blue light controls cell elongation and is an essential signal for the plant to adjust its growth to the surrounding light conditions [75]. Although light responses in horticultural crops differ between genotypes, enhanced amounts of UV light generally increase the thickness of the leaf cuticle [64], which in turn strengthens plant resistance to attacks from fungal pathogens [65,66]. However, for other species and under other exposure conditions, UV radiation can increase plant susceptibility to fungal pathogens [67,68]. A reduction in stem elongation as a result of UV exposure is often observed in greenhouse crops [76], which in turn modifies the plant microclimate. For example, UV-A and blue light increase shoot length and internode length in cucumber, but have the opposite effect on tomato and no effect on rose, while UV-A reduces stem length in rose and internode length in poinsettia [77,78,79,80,81]. Similarly, enrichment of natural and/or HPS light with blue and red light limits stem length in ornamental crops [82]. In combination, UV-B and blue light reduce leaf area in cucumber, leafy vegetables, and rose, while UV-B in combination with red light increases leaf area of pepper compared with monochromatic red light [56,80,83,84,85]. Blue light also increases leaf mass area, leaf and stem thickness, and shoot dry mass in cucumber [79,86,87], but reduces shoot dry mass in leafy vegetables [56,84], whereas UV-B increases leaf thickness in lettuce [85]. Plant responses to a light spectrum may be within a small wavelength interval. For example, it has been shown that 430–450 nm gives a greater leaf and stem growth increase in green perilla than 455–470 nm [88]. A combination of blue, red, and far-red light increases dry matter in cucumber and tomato compared with HPS lamps, particularly at a low blue:red ratio [89,90]. Exposure to UV light also alters epicuticular wax, which protects the plant against pathogen invasion [91]. Additionally, it induces morphological changes in trichomes of leaves [92]. Branching is often promoted by UV-B and blue light, while flowering induction, precocity, and duration are species-dependent. Furthermore, elevated parts of far-red light (lowered R:FR ratio) increase elongation of plants due to greater internode elongation [93], while a high R:FR ratio results in plants with a compact growth habit [58], creating a more shaded and moist leaf surface due to slower air movements within the canopy. However, plant ability to respond to R:FR ratio (e.g., via phytochromes PHYA, PHYB) is variety- and species-dependent. Leaf expansion can be promoted or inhibited by FR light [93,94], which may be related to competition for resources between the leaf and stem growth or auxin-induced cytokinin breakdown in leaf primordia. A low R:FR ratio may also decrease leaf mass per area and leaf duration, and cause leaf hyponasty and solar leaf tracking. Reduced branching in many species due to inhibition of bud outgrowth via phytohormones (i.e., auxin, strigolactones, cytokinins, ABA) has been observed under a low R:FR ratio. Flowering of many crops is accelerated under a low R:FR [58], but this varies according to the species [95].

4.1.2. Photosynthesis

Plant growth and metabolite accumulation depend on photosynthesis, which is suboptimal at very weak [96] or excessive light intensity [97]. Light intensity and light quality both have a very strong impact on plant photosynthesis, while daylength may affect the plant circadian clock and primary metabolism via cumulative carbon biomass. Plants modulate their photosynthesis pigments to the prevailing light spectrum and intensity. Although species-dependent, the chlorophyll (chl) content and the chl a/b ratio usually increase with blue light [77,86,98]. For different species, blue and red light increase the plant content of carotenoids, such as lutein and β-carotene, while UV may reduce it [84,89,99,100,101]. Blue light increases photosynthetic activity when used together with other wavelengths, but reduces it when used alone [77,84,86], whereas UV-B decreases plant photosynthesis efficiency [102]. Studies of several specific wavelengths (from 405 to 700 nm) on photosynthesis of tomato, lettuce, and petunia plants have revealed higher photosynthesis with the blue region (range 417–450 nm) and red region (range 630–680 nm) than the green region (501, 520, 575, 595 nm) [103]. A blue and red light combination allows for higher photosynthetic activity than monochromatic light of either, which can be harmful for plants [104,105]. Opening of the stomata, which are a natural entry point for leaf microorganisms, is driven by blue light, although red light also promotes stomatal opening. Blue light is also involved in chloroplast movement within the cell to increase photosynthetic ability under different light conditions. An increased number of stomata and length of palisade tissue cells have been observed under blue light compared with red or green light [87]. Higher numbers of grana lamellae and more stacked thylakoid membranes have been observed in cucumber grown under low blue light radiation [98]. Blue light also prevents accumulation in the chloroplasts of starch grains, which block the incoming light. In addition to its effect on leaf area, leaf orientation, and leaf branching, thereby modifying crop photosynthesis, a low R:FR ratio may reduce stomatal conductance, stomatal density, chlorophyll content, chloroplast development, thylakoid structure and protein composition, and the activity of some enzymes of the Calvin cycle [58]. As FR light negatively affects root hair density, mycorrhizal colonization, and ATP formation, the R:FR ratio influences plant mineral nutrition. Moreover, a low R:FR ratio promotes nutrient allocation to the shoot at the expense of roots [58].

4.1.3. Primary and Secondary Metabolism

The light spectrum also influences the accumulation of plant primary and secondary metabolites [106]. For example, accumulation of soluble sugars, starch, soluble protein, and polyphenols is higher when crops are grown under monochromatic red or blue than white light [107,108,109,110,111,112,113], which may impact the phyllobiome. Indeed, the phyllosphere microbiota uses leaf surface resources, such as amino acids, carbohydrates, and organic acids, passively leaked by plants [114]. A combination of red, blue, and white light enhances soluble sugar and nitrate concentrations in basil plants [115]. However, a low R:FR ratio downregulates the activity of the key enzymes involved in nitrogen assimilation (nitrate reductase, nitrite reductase, and glutamine synthase), which may impact cell metabolism [58]. Blue light and mixtures of red, blue, and green light increase ascorbic acid accumulation in leafy vegetables [84,116,117], while UV-A may reduce ascorbic acid content [118]. Anthocyanin leaf content is usually promoted by UV-A, UV-B, and blue light [75]. In particular, UV-A, blue, and red light increase the anthocyanin level in leafy vegetables, while green light reverses blue-light-induced anthocyanin accumulation [94,118,119,120]. Sulfur-containing secondary metabolites, such as glucosinolate, which can protect the plant against predation and pathogens, may also be promoted by blue light or a mixture of red, blue, and green light [121,122,123]. The R:FR ratio also impacts accumulation of phenolics in different species [115,124]. In addition, light affects the synthesis, profile, and emission of volatile organic compounds (VOCs) by plants, which increases plant attractiveness to plant parasitoids and orientation of predators [124,125]. Release of VOCs from leaves increases when they are exposed to UV, white light, or a low R:FR ratio, although this effect may be species-specific.

4.1.4. Plant Defense Mechanisms

Light, such as UV-B, affects several plant hormones, notably jasmonate (involved in response to attack by necrotrophic pathogens) and salicyclic acid (involved in response to attack by biotrophic microbial pathogens), that coordinate the plant immune response to environmental stresses [66]. Blue light also induces pathogenesis-related gene expression [126], while red light induces salicylic acid content and expression of salicylic-acid-regulating PR-1 and WRKY genes in pathogen-inoculated cucumber plants [127,128]. On the other hand, a low R:FR ratio resulting in high plant population or plant shading may affect plant immunity, which has been linked in some species to reduced transcription of salicylic-acid-responsive genes or to decreased jasmonate sensitivity and reduced biosynthesis of tryptophan-derived secondary metabolites [129,130]. In particular, a low R:FR ratio inhibits salicylic acid and jasmonic-acid-mediated disease resistance in Arabidopsis plants [130,131]. Furthermore, a low R:FR ratio may induce high levels of gibberellin and auxin, which are involved in internode elongation, while gibberellin and ethylene are implicated in petiole extension [58,132].
Light spectrum has a strong effect on the antioxidant properties of horticultural plants [109,110,133,134,135,136]. For example, UV-B light can cause plant DNA damage, resulting in a cascade of protective events, such as flavonoid synthesis and expression of chalcone synthase genes and photolyase genes [75]. However, UV-B may have no effect or may reduce flavonoid accumulation in some species [100]. Compared with white light, blue and red light increase the activity of various reactive oxygen species (ROS)-scavenging enzymes and reducing substances (reduced glutathione (GSH) and ascorbic acid (ASA)) [137], which play an important role in plant defense mechanisms against plant pathogens in species such as tomato [138]. In tomato, blue light promotes leaf accumulation of proline, polyphenolic compounds, and antioxidants, and ROS scavenger activities, which might be partly related to inhibition of gray mold disease. On the other hand, red- and green-light-treated tomato plants have been shown to exhibit lower proline content [110]. Light of specific wavelengths (UV, blue, red) also promotes synthesis of stilbenic compounds compared with white light [46,139,140]. Stilbenes, which are low-molecular-weight phenolics, play an important role in plant defense responses by overcoming fungal pathogen attacks [110,141]. Similarly, red light induces cinnamic acid synthesis and increases plant resistance via the tryptophan and phenylpropanoid pathways [142]. Moreover, high gamma-aminobutyric acid levels are promoted by plant UV-B exposure, resulting in higher bacterial diversity in the phyllosphere and lower plant resistance to fungal disease [143]. On the other hand, plants exposed to a low R:FR are more sensitive to pathogens due to changes in leaf morphology, chlorophyll content, and downregulation of jasmonate and salicylic acid [58,66].

4.2. Direct Plant–Microbe Interactions Induced by Light

Physiological changes in the plant caused by different light qualities have a major impact on the phyllosphere microbiota. In sunflower plants grown under HPS lamps, white LEDs, or red:blue (80:20 ratio) LEDs, it has been shown that the fungal communities are more affected than the bacterial communities by different light qualities [51]. Although that study did not investigate whether the effects on the microbiota are direct or indirect, other research (presented below) suggests that the effect is often caused by physiological alterations in the plant.

4.2.1. Leaf Leachate

The availability of organic carbon as a prerequisite for microbial colonization in the phyllosphere has been surveyed in several reviews [28,30,36,37]. Microbial phyllosphere communities are limited first by availability of organic carbon sources and only second by availability of organic nitrogen sources [37]. Although the phyllosphere is often characterized as a habitat lacking in nutrients, leaves exude a wide range of carbon compounds, such as carbohydrates, amino acids, organic acids, and sugar alcohols [30]. The availability of these nutrients is highly dependent on photosynthesis, which in turn is highly dependent on light quality and intensity. Leaching of nutrients across the leaf surface occurs in the presence of liquid water, but can also be increased by the phyllosphere microbiota through microbially produced biosurfactants [28]. The most abundant compounds in leachate are photosynthetic compounds, such as glucose, fructose, and sucrose [144,145]. However, the glandular trichomes, which are important sites of leaching, also secrete proteins, oils, secondary metabolites, and mucilage [36,146,147,148]. Use of red, or red plus blue, LED light has been shown to increase the amount of soluble sugars and proteins in a wide range of plants, as mentioned earlier. This physiological change in the plant, caused by choice of artificial light source, changes the carrying capacity of the leaf and governs which microorganisms are favored by the increase or decrease in compounds specific for their survival. While the microbial community as a whole can utilize a wide range of compounds for colonization and growth, a single microbial species can be quite specific in its metabolism. For example, substrate profiling of Pseudomonas syringae has shown that this bacterium uses a restricted number of sugars, organic acids, and amino acids [149]. This implies that, with increased knowledge of the metabolic patterns of specific microorganisms, light could be used as a management tool, not only for plant growth, but also in order to favor microbial species of importance.

4.2.2. Light-Triggered Pathways

While light within the spectral wavelength from 300 to 800 nm can have an effect on plant growth and development, red light seems to have the largest impact relating to defense against microbial pathogens by triggering both plant defense genes and hormonal pathways. The composition of the phyllosphere microbial community is driven by a wide range of factors. However, the plant immune system is thought to play a major role in shaping the community composition. It has been shown that triggering of the salicylic acid pathway leads to reductions in both diversity and population sizes of endophytic bacteria, while epiphytic bacteria are not measurably affected, and that Arabidopsis thaliana plants deficient in the jasmonic acid pathway host a greater epiphytic bacterial community diversity [150]. For horticultural species, red and green light have a positive effect on tomato seedlings, with less infection by Pseudomonas cichorii JBC1 compared with white light or dark treatment [151]. A similar result was observed for cucumber plants infected with powdery mildew (Sphaerotheca fuliginea) and exposed to red light, while no effect was found under green light [128]. This decrease in infection level was related to the upregulation of the defense gene phenylalanine ammonia lyase (PAL) and pathogenesis-related protein 1a (PR1a) under red or green light treatments [151]. This leads to the conclusion that light significantly alters the activation of defense-related genes. Differences in results between different studies, however, imply that use of light treatment for control of pathogens has to be customized to the plant–pathogen system.
Downregulation of the salicylic acid and jasmonic acid pathways when plants compete for light against other plants (i.e., a low R:FR ratio) means that the plants become more sensitive to pathogen attack, as shown with Botrytis cinerea in Arabidopsis [129]. This plant response to a low R:FR ratio has also been reported elsewhere [130]. A low R:FR ratio can be avoided in the greenhouse by spacing out the plants, allowing for more light to enter the lower parts of the canopy. While a high R:FR ratio leads to pathogen susceptibility, use of red light leads to activation of the salicylic acid pathway-mediated systemic acquired resistance (SAR) in Arabidopsis, making the plant more resistant to Pseudomonas syringae pv. tomato [152]. A study on rice has also shown increased resistance to disease, specifically Bipolaris oryzae, when rice plants are subjected to red light, with an increasing level of resistance being demonstrated with an increasing dose of red light [142]. However, in rice plants, disease resistance is mediated through the tryptophan and phenylpropanoid pathways, and not by the salicylic acid pathway as suggested in Arabidopsis.

4.2.3. Changes in Leaf Physiological Characteristics

Leaf surface properties have a large impact on the establishment and survival of phyllosphere microorganisms [36]. The thickness of the adaxial epidermis layer has been found to be one of the three most important leaf attributes governing the plant–microbe system, where an epidermal layer thicker than 20.77 µm results in lower microbial colonization rates [153].
Changes in epicuticular wax layers and epidermal tissues, in particular, can emerge as consequences of subjecting plants to different light qualities [127]. A difference in effect on leaf morphological characteristics depending on light quality has also been seen between sun-exposed and shaded leaves, with sun-exposed leaves having a thicker cuticle than shaded leaves [154]. It has been suggested that UV-B radiation is the factor responsible for a thicker cuticular wax layer on the leaf surface, with e.g., increased irradiation with UV-B, increasing the wax layer in cucumber, pea, and barley by 25% [155]. A thicker wax layer prevents, or at least delays, pathogen infection, especially for fungal pathogens that use direct penetration as a means of infection. In a detached leaf assay using soybean, it has been shown that disease severity of soybean rust (Phakopsora pachyrizi) is negatively correlated with amount of epicuticular wax and that the leaves at the top of the canopy have a higher amount of wax than leaves in middle and lower levels [91].

5. Light-Quality-Mediated Effects on the Leaf Microbiota

Biofilm is a natural way for microorganisms to co-exist on a surface or interface, enclosed in a exopolysaccharide matrix produced by the microbes themselves [156]. Regardless of whether the microorganisms concerned are human or plant pathogens or microbes used as biocontrol agents (BCA), their efficiency depends on how well they establish and survive on a surface. Environmental factors, such as temperature, humidity, and light, are important factors that shape microbial communities. Biofilms protect microbes against antibiotics and harsh environmental factors and maintain nutrient availability [156]. To date, bacteria have been regarded as non-phototrophic organisms and insensitive to light. Only phototrophic bacteria were known to react and respond to light. However, light has been shown to affect bacterial decisions to change from a planktonic single cell motile lifestyle to a surface-attached lifestyle in a multicellular community as biofilm [157]. This is supported by the fact that some of the photo receptor proteins also control mechanisms involved in biofilm formation and these receptors are linked to the GGDEF and EAL protein domains, which are involved in the transition from a planktonic to a sessile life style [158].

5.1. Leaf Pathogens

Irrespective of their growing site (nature, field stand, or controlled environment), plants can be attacked by plant diseases. Amongst the fungal pathogens, grey mold (Botrytis cinerea), powdery mildew (Podosphaera spp.), and downy mildew (Peronospora spp.) are often reported in major greenhouse crops, such as tomatoes, cucumber, strawberries, and ornamental plants (e.g., grey mold in tomato [110]; powdery mildew in strawberries (Fragaria X ananassa), [159,160] and roses (Rosa spp.) (P. pannosa) [49]; downy mildew (Pseudoperonospora cubensis) in cucumber [47]). Different bacterial species, for example Xanthomonas spp. and Pseudomonas spp., can also cause severe damage to plants [50,161,162]. The idea of using light as a strategy to control leaf pathogens is not new, e.g., 20 years ago, greenhouse experiments with blue-pigmented photoselective sheets showed that these inhibited sporulation and colonization of downy mildew on cucumber [47]. Light regulates biofilm formation, attachment, motility, and virulence of both fungal and bacterial plant pathogens (Table 2), factors which are crucial for establishment on the leaf surface.
Implementation of LED light as an environmentally friendly tool in indoor production has increased in recent years. In this context, it has been shown that light quality has an impact on growth and development of the conidia of P. pannosa, which causes powdery mildew disease on roses [49]. Blue light (420–520 nm) was observed to decrease conidial growth in that study, while far-red light (575–675 nm) had the opposite effect, i.e., it increased pathogen growth. However, the same study could not demonstrate a reduction in conidia development when roses were grown with 18 h daylight complemented with 6 h of blue or red light [49]. Exposure to blue light has been demonstrated to increase the antioxidant and polyphenolic content in tomato plants and thereby control the attachment of Botrytis cinerea [110]. Moreover, a study on cucumber plants indicated that light quality affects incidence of powdery mildew and expression of defense-related genes [127]. Bacterial infection in plants can also be suppressed by light of different quality, e.g., green light reduces phytotoxic lipopeptide and siderophore production in Pseudomonas cichorii, which might affect survival of this plant pathogen [167]. In Xanthomonas spp., light quality has a negative impact on motility, and, thus, host colonization [161,162]. Swarming motility in Pseudomonas syringae is suppressed under light conditions (white, blue, red plus far-red) compared with dark treatment, but different light qualities (white, blue, red plus far-red) also have differing effects, with blue light promoting swarming motility [50].

5.2. Microbial Biocontrol Agents

As is the case for deleterious microorganisms, such as pathogens, plant-health-promoting biocontrol agents are also affected by the light regime provided under controlled conditions. A successful BCA should exhibit (i) several antifungal or antibacterial (antagonistic) properties, (ii) ability to spread on the plant surface after application, and (iii) capacity to establish in existing biofilms. However, very little is known about how different light regimes affect BCA when it comes to establishment in the plant canopy. One study demonstrated that, in Serratia marcescens, antibiotic pigment prodigiosin concentration in bacterial cells decreases under white and blue light (470 nm) conditions, but growth is not affected [168]. The same study showed that red and far-red light have no effect on the concentration of prodigiosin [168]. Another study [170] isolated the photolyase gene (phr1) from Trichoderma harzianum, a common soil fungus used as a BCA against phytopathogenic fungi [171] and investigated expression of phr1 when exposed to blue light. Their results showed that gene expression of photolyase (phr1) is induced very rapidly in both mycelia and conidiphores, and that light induces development of pigmented resistance spores as well as expression of phr1 [159]. Bacillus amyloliquefaciens is another BCA often used in horticulture against soilborne and post-harvest pathogens. In this species, all light quality except blue light affects growth, swarming motility, biofilm formation, and antifungal activity positively [164]. Red light (645 nm) increases biocontrol efficacy and colonization of BCA on fruit surfaces, while blue light (458 nm) has a negative impact on growth, motility, and biofilm formation [164].

5.3. Molecular Interactions

For many years, only phototrophs were considered to respond to light in order to find an optimally illuminated environment for harvesting solar energy [172]. However, the increasing number of papers on bacterial whole genome sequencing has now revealed a large number of putative genes coding for photoreceptor proteins distributed among several taxa. During bacterial evolution, bacteria have evolved photoreceptor proteins that can detect visible light in the environment, in order to protect themselves from damaging UV radiation [172]. Bacteria can also respond to light by switching between the single cell planktonoic lifestyle and the multicellular life style of bacterial communities known as biofilms [173]. Six classes of photoreceptors have been identified in the bacteria photosensory system, based on their structure of their chromophore. These are: cryptochrome, rhodopsin, phytochrome, photoactive yellow protein (PYP), light oxygen voltage receptor protein (LOV), and blue light sensing protein using FAD (BLUF) [172].
Cyclic di-guanosine monophosphate (c-di-GMP), a key role player in the bacterial signal transduction system, regulates bacterial behaviors, such as biofilm formation, virulence, and production of adhesion proteins [174]. It is produced from diguanylate cyclases (DGCs) and is then broken down to 5′-phosphoguanylyl-(3′-5′)-guanosine (pGpG) through hydrolysis by phosphodiesterases (PDEs). Of these, DGCs are associated with the GGDEF photoreceptor domain and PDEs with the EAL domain [175]. Both are involved in light-sensing processes, together with the LOV and BLUF domains [157,158].
Two photoreceptors are involved in blue light sensing in plants and in microbes, namely LOV and BLUF. Both these protein domains have been shown to control attachment, multicellularity, production of adhesion proteins, and virulence (Table 2). Therefore, blue light has been shown to be a promising candidate to combat bacterial and fungal infections in medical science. For example, several studies have reported bactericidal effects on Pseudomonas aeruginosa and Staphylococcus aureus when exposed to 405 nm light [169]. Furthermore, exposure of methicillin-resistant Staphylococcus aureus to 405 and 470 nm light has been shown to bring about a significant reduction in growth [176]. Similar findings have been made in a study on bacteria involved in clinical infections, where both planktonic and bacterial biofilm proved susceptible to blue light, with significant reductions in viability for all tested strains [177]. Blue light exposure in horticulture has been shown to have negative effects on both bacteria and fungi (Table 2). However, blue light conditions have been reported to enhance disease attack caused by the fungus Sphaerotheca fuliginea [127]. In Pseudomonas syringae, it has been demonstrated that light decreases the swarming motility and that this is regulated by bacteriophytochrome and LOV-HK (Light Oxygen Voltage-Histidine Kinase) [50]. In the plant pathogen Xanthomonas axonopodis, LOV is activated by blue light and may be involved in the control of bacterial virulence [161].
All these studies show that light quality has an impact, one way or another, on the behavior of microorganisms. For this to occur, the organism needs to perceive and transmit the signal, which is done by photosensory proteins. As mentioned above, the BLUF and LOV photoreceptor domains are involved in blue light sensing. The LOV domain belongs to the PAS (Per-ARNT-Sim) superfamily connected in a network of conserved domains (GGDEF, EAL, PAS, GAF (cGMP-specific phosphodiesterases, adenylyl cyclases and FhlA), HK, HisKA (histidine protein kinases), and STAS (sulfate transporter and anti-sigma factor antagonist)) [178]. A very extensive bioinformatics study of photoreceptors across kingdoms has been conducted [178]. According to their data for bacteria, different groups of protein architecture dominate across different phyla. Within the Proteobactería, the combinations EAL-GAF-GGDEF-LOV-PAS and EAL-GGDEF-HAMP-LOV-PAS are the most abundant architectures of photoreceptor proteins, together with HATP-HisKA-LOV. Within the Firmicutes, the combination STAS-LOV is the most common architecture. Across all investigated phyla [169], there are short (150 aa) LOV proteins that can stand alone with a highly conserved motif of five amino acids with a cysteine at position 54 that forms the cysteine–flavin assembly during the LOV photocycle, which is also involved in sensing blue light [179]. The BLUF domain control functions such as photosystem synthesis, biofilm formation, and both swarming and twitching motility [180,181]. It is widespread across the bacterial kingdom, but in anoxygenic and plant-associated species BLUF proteins are not as abundant as LOV proteins. For example, BLUF proteins have not been recovered from Firmicutes, Chloroflexi, or EuArchaea, which instead only carry genes encoding LOV proteins [158]. In many species, BLUF seems to act alone. In Escherichia coli, Klebisella pneumoniae, and Magnetococcus sp., BLUF is combined with EAL [158,173]. The BLUF-EAL protein YcgF in E. coli acts as a direct anti repressor in a blue light response, which in turn activates other proteins important for biofilm formation [182].
Photoactive yellow protein (PYP) is a blue light sensor protein first discovered in halophilic purple phototrophic bacteria [183]. With the increasing number of whole genome sequencing studies, there have been reports of PYP proteins in bacteria other than phototrophs, mostly within in Proteobacteria [184]. Photoactive yellow protein is small, only 125 amino acids long, and is often present as part of the PAS domain [185]. Studies have shown that PYP serves as a photosensor for negative phototaxis [186].

6. Discussion

Day length, light intensity, and light quality affect plant architecture and morphology, plant growth, and plant development. Lighting is a crucial tool for greenhouse horticulture and plant production in controlled environments. It plays a central role for the microclimate in the crop stand, e.g., temperature and relative humidity. Light-related effects on the crop can be direct or indirect. The potential of the plant microbiome to influence crop growth and development and the ability to withstand abiotic and biotic stress has been repeatedly highlighted [28,187,188]. Microbiome-based tools and prediction models have been suggested [187]. Despite the importance of light and illumination in greenhouse horticulture (Figure 2 and Figure 3) and the increasing interest in the phyllosphere microbiome, light-associated factors are only occasionally receiving the attention they deserve in experimental settings or in applied contexts (Figure S3).
At present, knowledge on the influence of light, especially light quality, on phyllosphere–microbe interactions resembles a random mosaic in an otherwise vast field, as previous studies have tended to consider either the behavior of a specific target organism or expression of a light-related gene or receptor, or big metagenomics datasets with limited functional information. To bring phyllosphere studies within the scope of ecological principles and theories, the presence and also the function of microorganisms need to be highlighted. However, it is of utmost importance to discriminate between mechanisms and processes that can be abstracted and those that cannot. In this context, the pathosystem deserves particular attention. In the present literature review, we focused on interactions between selected plant and human pathogens and light quality and considered some of the molecular mechanisms involved. However, in planta studies are rare and often lack sufficient characterization of the growing environment. To understand the interactions between light, especially light quality, plant/crop stand, and microbiome, critical experimental conditions and physiological processes need to be continuously monitored. This requires such disciplines as crop physiology and microbiology/plant pathology to engage with common phenotypic platforms.
The composition and amount of microbially available organic nutrients, a suitable microclimate with respect to temperature and humidity/moisture, and niches providing shelter from deleterious irradiation and unintentional predation are key properties of a suitable microbial phyllosphere environment. Thus, mechanisms affecting these key properties will decide colonization density and composition. Light quality directly or indirectly influences many of these processes (see Figure 2). In this regard, nutrient sources available in the phyllosphere can serve as an example. A few studies have examined the composition and quantity of leaf lysates [144,189,190] and interactions between organic nutrients and microbial proliferation [145]. Two recent studies considering almost 400 different nutrient sources have indicated that the nutritional preferences of some phyllosphere colonizers change in the presence of different light qualities [52,53]. The utilization of compounds themselves, but also their use within carbon, nitrogen, or sulfur metabolism, is moderated in the presence of different light qualities, and, consequently, the secondary metabolites are also moderated. At present, the focus has been on light qualities of major importance for plant photosynthetic activity (blue, red) in such studies. To the best of our knowledge, the impact of other light spectra on microbial utilization of nutrients has not been investigated. Such information, as well as transcriptomics data on the phyllosphere microbial community, needs to be provided, along with plant and environmental monitoring data, in order to reveal the impact of light quality and to assess the potential of light as a tool for habitat management.
The deleterious impact of certain light qualities on plant pathogenic fungi has been investigated since the late 1990s [47], with particular focus on commercially important pathogens (e.g., grey mold and powdery and downy mildew). In contrast to studies on bacteria, these fungi studies primarily concentrate on the disease incidence, while rarely analyzing underlying molecular mechanisms. Such information is needed for non-pathogenic and pathogenic fungi (for endophytic and ectophytic phyllosphere bacteria) in order to implement light quality strategies into greenhouse horticulture and controlled environment production systems. Overall, studies on new, non-chemical control strategies for leaf pathogens are of substantial interest in the development of sustainable horticultural indoor production systems.
It has been suggested that the phyllosphere be used as a platform for the testing of ecological principles [77]. Different literature reviews [187,188] have proposed ecological theories and principles relating to the phytobiome. Given a multidisciplinary and systematic approach, the theories and principles depicted in Table 3 could contribute to a better understanding of light–phyllosphere interactions in greenhouse horticulture and to the development of sustainable growing practices.

Supplementary Materials

The following are available online at Figure S1: Relative spectral output from three different light sources: HPS lamps (Philips Master 400 W), fluorescent tubes (Sylvania TLD840 58 W), and LED lights (Valoya B150, spectrum AP673L 144 W). Figure S2: Number of publications considering the topic ‘supplementary lighting in greenhouse horticulture’. The literature search considered three keyword combinations, namely artificial lighting*greenhouse*horticulture (102 publications), supplementary lighting*greenhouse*horticulture (201 publications), and artificial illumination*greenhouse*horticulture (21 publications) and was performed in Web of Knowledge (WoK) using all WoK databases (Web of Science Core Collection, Biosis Citation Index, CABI, Current Contents Connect, Data Citation Index, Derwent Innovation Index, KCI-Korean Journal Database, MEDLINE, Russian Science Citation Index, SciELO Citation Index, Zoological Record). The literature search was restricted to 30 years (1988–2018) (dates of performance: November 19 and 20, 2018). Figure S3: Description of light conditions in study output considering the keyword combination “phyllosphere*greenhouse*horticulture”. The search was restricted to 30 years (1988–2018) and entailed 27 publications conducted under greenhouse, climate chamber, or polytunnel. The survey was performed in Web of Knowledge (WoK) using all WoK databases (Web of Science Core Collection, Biosis Citation Index, CABI, Current Contents Connect, Data Citation Index, Derwent Innovation Index, KCI-Korean Journal Database, MEDLINE, Russian Science Citation Index, SciELO Citation Index, Zoological Record). Values indicate percentage of studies stating or avoiding information on environmental conditions (relative humidity, temperature), light conditions (day length, light intensity) and use of supplementary lighting, as well as control of description of light spectrum in the plant stand. The proportion of publications discussing the impact of light on the results obtained was also determined (3.9% corresponds to one publication) (dates of performance: November 19 and 20, 2018).

Author Contributions

All authors were involved in writing the original draft, draft preparation, and reviewing and editing this article. In detail, the authors took on the following responsibilities: conceptualization: B.A. and M.D.; methodology: B.A.; formal analysis: all authors; writing (in alphabetical order of surname): original draft preparation, B.A., K.J.B., M.D., M.K., S.K., A.K.R., T.N., writing, review and editing, B.A., K.J.B., M.D., M.K., S.K., A.K.R., T.N.; visualization: B.A., K.J.B., M.D.; project administration: B.A.; funding acquisition: B.A. (PI) in collaboration with M.K. and K.J.B.


This research was funded by Stiftelsen Lantbruksforskning and the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning, both Stockholm, Sweden, grant number R-18-25-006 (“Optimized integrated control in greenhouse systems sees the light”; PI: Beatrix Alsanius).

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analysis, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.


  1. Aleklett, K.; Hart, M.; Shade, A. The microbial ecology of flowers: An emerging frontier in phyllosphereresearch. Botany 2014, 92. [Google Scholar] [CrossRef]
  2. Andreote, F.D.; Gumiere, T.; Durrer, A. Exploring interactions of plant microbiomes. Sci. Agric. 2014, 71, 528–539. [Google Scholar] [CrossRef]
  3. Beilsmith, K.; Thoen, M.P.M.; Brachi, B.; Gloss, A.D.; Khan, M.H.; Bergelson, J. Genome-wide association studies on the phyllosphere microbiome: Embracing complexity in host-microbe interactions. Plant J. 2018, 97, 164–181. [Google Scholar] [CrossRef] [PubMed]
  4. Berg, G.; Grube, M.; Schloter, M.; Smalla, K. Unraveling the plant microbiome: Looking back and future perspectives. Front. Microbiol. 2014, 5, 148. [Google Scholar] [CrossRef]
  5. Brader, G.; Compant, S.; Vescio, K.; Mitter, B.; Trognitz, F.; Ma, L.J.; Sessitsch, A. Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Ann. Rev. Phytopathol. 2017, 55, 61–83. [Google Scholar] [CrossRef] [PubMed]
  6. Bringel, F.; Couee, I. Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front. Microbiol. 2015, 6, 486. [Google Scholar] [CrossRef] [PubMed]
  7. Bulgarelli, D.; Schlaeppi, K.; Spaepen, S.; van Themaat, E.V.L.; Schulze-Lefert, P. Structure and functions of the bacterial microbiota of plants. Ann. Rev. Plant Biol. 2013, 64, 807–838. [Google Scholar] [CrossRef] [PubMed]
  8. Carvalho, S.D.; Castillo, J.A. Influence of light on plant-phyllosphere interaction. Front. Plant Sci. 2018, 9, 1482. [Google Scholar] [CrossRef] [PubMed]
  9. Chaudhary, D.; Kumar, R.; Sihag, K.; Rashmi; Kumari, A. Phyllospheric microflora and its impact on plant growth: A review. Agric. Rev. 2017, 38, 51–59. [Google Scholar] [CrossRef]
  10. Farre-Armengol, G.; Filella, I.; Llusia, J.; Penuelas, J. Bidirectional interaction between phyllospheric Microbiotas and plant volatile emissions. Trends Plant Sci. 2016, 21, 854–860. [Google Scholar] [CrossRef]
  11. Finkel, O.M.; Castrillo, G.; Paredes, S.H.; Gonzalez, I.S.; Dangl, J.L. Understanding and exploiting plant beneficial microbes. Curr. Opin. Plant Biol. 2017, 38, 155–163. [Google Scholar] [CrossRef] [PubMed]
  12. Gao, S.; Liu, X.; Dong, Z.; Liu, M.; Dai, L. Advance of phyllosphere microorganisms and their interaction with the outside environment. Plant Sci. J. 2016, 34, 654–661. [Google Scholar]
  13. Iguchi, H.; Yurimoto, H.; Sakai, Y. Interactions of methylotrophs with plants and other heterotrophic bacteria. Microorganisms 2015, 3, 137–151. [Google Scholar] [CrossRef] [PubMed]
  14. Jackson, C.R.; Stone, B.W.G.; Tyler, H.L. Emerging perspectives on the natural microbiome of fresh produce vegetables. Agriculture 2015, 5, 170–187. [Google Scholar] [CrossRef]
  15. Kowalchuk, G.A.; Yergeau, E.; Leveau, J.H.J.; Sessitsch, A.; Bailey, M. Plant-Associated Microbial Communities. In Environmental Molecular Microbiology; Lui, W.-T., Jansson, J., Eds.; Caister Academic Press: Norfolk, UK, 2010; pp. 131–148. [Google Scholar]
  16. Lemanceau, P.; Barret, M.; Mazurier, S.; Mondy, S.; Pivato, B.; Fort, T.; Vacher, C. Plant communication with associated microbiota in the spermosphere, rhizosphere and phyllosphere. Adv. Bot. Res. 2017, 82, 101–133. [Google Scholar] [CrossRef]
  17. Leveau, J.H.J. Microbiology Life on leaves. Nature 2009, 461, 741. [Google Scholar] [CrossRef] [PubMed]
  18. Markland, S.M.; Kniel, K.E. Human pathogen-plant interactions: Concerns for food safety. Adv. Bot. Res. 2015, 75, 115–135. [Google Scholar] [CrossRef]
  19. Meyer, K.M.; Leveau, J.H.J. Microbiology of the phyllosphere: A playground for testing ecological concepts. Oecologia 2012, 168, 621–629. [Google Scholar] [CrossRef]
  20. Mueller, D.B.; Schubert, O.T.; Roest, H.; Aebersold, R.; Vorholt, J.A. Systems-level Proteomics of Two Ubiquitous Leaf Commensals Reveals Complementary Adaptive Traits for Phyllosphere Colonization. Mol. Cell. Proteom. 2016, 15, 3256–3269. [Google Scholar] [CrossRef]
  21. Mueller, T.; Ruppel, S. Progress in cultivation-independent phyllosphere microbiology. Fems Microbiol. Ecol. 2014, 87, 2–17. [Google Scholar] [CrossRef]
  22. Muller, D.B.; Vogel, C.; Bai, Y.; Vorholt, J.A. The plant microbiota: Systems-level insights and perspectives. Ann. Rev. Genet. 2016, 50, 211–234. [Google Scholar] [CrossRef] [PubMed]
  23. Rastogi, G.; Sbodio, A.; Tech, J.J.; Suslow, T.V.; Coaker, G.L.; Leveau, J.H.J. Leaf microbiota in an agroecosystem: Spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 2012, 6, 1812–1822. [Google Scholar] [CrossRef] [PubMed]
  24. Remus-Emsermann, M.N.P.; Tecon, R.; Kowalchuk, G.A.; Leveau, J.H.J. Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere. ISME J. 2012, 6, 756–765. [Google Scholar] [CrossRef] [PubMed]
  25. Saikkonen, K.; Mikola, J.; Helander, M. Endophytic phyllosphere fungi and nutrient cycling in terrestrial ecosystems. Curr. Sci. 2015, 109, 121–126. [Google Scholar]
  26. Schlaeppi, K.; Bulgarelli, D. The plant microbiome at work. Mol. Plant Microbe Interact. 2015, 28, 212–217. [Google Scholar] [CrossRef] [PubMed]
  27. Thapa, S.; Prasanna, R. Prospecting the characteristics and significance of the phyllosphere microbiome. Ann. Microbiol. 2018, 68, 229–245. [Google Scholar] [CrossRef]
  28. Vacher, C.; Hampe, A.; Porte, A.J.; Sauer, U.; Compant, S.; Morris, C.E. The phyllosphere: Microbial jungle at the plant-climate interface. Ann. Rev. Ecol. Evol. Syst. 2016, 47, 1–24. [Google Scholar] [CrossRef]
  29. Vogel, C.; Bodenhausen, N.; Gruissem, W.; Vorholt, J.A. The Arabidopsis leaf transcriptome reveals distinct but also overlapping responses to colonization by phyllosphere commensals and pathogen infection with impact on plant health. New Phytol. 2016, 212, 192–207. [Google Scholar] [CrossRef] [PubMed]
  30. Vorholt, J.A. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 2012, 10, 828–840. [Google Scholar] [CrossRef]
  31. Vorholt, J.A. The phyllosphere microbiome: Responses to and impacts on plants. Phytopathology 2014, 104, 155. [Google Scholar]
  32. Whipps, J.M.; Hand, P.; Pink, D.; Bending, G.D. Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol. 2008, 105, 1744–1755. [Google Scholar] [CrossRef] [PubMed]
  33. Yang, T.; Chen, Y.; Wang, X.X.; Dai, C.C. Plant symbionts: Keys to the phytosphere. Symbiosis 2013, 59, 1–14. [Google Scholar] [CrossRef]
  34. Beattie, G.A.; Lindow, S.E. The secret life of bacterial pathogens on plants. Ann. Rev. Phytopathol. 1998, 33, 145–172. [Google Scholar] [CrossRef] [PubMed]
  35. Beattie, G.A.; Lindow, S.E. Bacterial colonization of leaves: A spectrum of strategies. Phytopathology 1999, 89, 353–359. [Google Scholar] [CrossRef] [PubMed]
  36. Leveau, J.H.J. Microbial communities in the phyllosphere. In Biology of the Plant Cuticle; Riederer, M., Müller, C., Eds.; Blackwell Publishing: Oxford, UK, 2006; pp. 334–367. [Google Scholar]
  37. Lindow, S.E.; Brandl, M.T. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 2003, 69, 1875–1883. [Google Scholar] [CrossRef] [PubMed]
  38. Diaz, B.M.; Biurrun, R.; Moreno, A.; Nebreda, M.; Fereres, A. Impact of ultraviolet-blicking plastic films on insect vectors of virus diseases infesting crisp lettuce. HortScience 2006, 41, 711–716. [Google Scholar] [CrossRef]
  39. Hemming, S. Use of natural and artificial light in horticulture—Interaction of plant and technology. Acta Hortic. 2011, 907, 25–36. [Google Scholar] [CrossRef]
  40. Stamps, R.H. Use of colored shade netting in horticulture. HortScience 2009, 44, 239–241. [Google Scholar] [CrossRef]
  41. Philips. Master Agro 400W E40 1SL/12. 2018. Available online: (accessed on 7 January 2019).
  42. Philips. Master HPI-T Plus 400 W/643. Philips Lighting Holding B.V. 2018. Available online: (accessed on 7 January 2019).
  43. Heliospectra. Heliospectra EOS. Heliospectra AB: 2018. Available online: (accessed on 7 January 2019).
  44. Senmatic. Senmatic FL300. Senmatic A/S: 2018. Available online: (accessed on 7 January 2019).
  45. Valoya. Valoya Product Brochure. Valoya Oy: 2018. Available online: (accessed on 7 January 2019).
  46. Ahn, S.Y.; Kim, S.A.; Yun, H.K. Inhibition of Botrytis cinerea and accumulation of stilbene compounds by light-emitting diodes of grapevine leaves and differential expression of defense-related genes. Eur. J. Plant Pathol. 2015, 143, 753–765. [Google Scholar] [CrossRef]
  47. Reuveni, R.; Raviv, M. Control of downy mildew in greenhouse-grown cucumbers using blue photoselective polyethylene sheets. Plant Dis. 1997, 81, 999–1004. [Google Scholar] [CrossRef]
  48. Suthaparan, A.; Stensvand, A.; Solhaug, K.A.; Torre, S.; Telfer, K.H.; Ruud, A.K.; Mortensen, L.M.; Gadoury, D.M.; Seem, R.C.; Gislerød, H.R. Suppression of cucumber powdery mildew by supplemental UV-B radiation in greenhouses can be augmented or reduced by background radiation quality. Plant Dis. 2014, 98, 1349–1357. [Google Scholar] [CrossRef] [PubMed]
  49. Suthaparan, A.; Stensvand, A.; Torre, S.; Herrero, M.L.; Pettersen, R.; Gadoury, D.M.; Gislerød, H.R. Continuous lighting reduces conidial production and germinability in the rose powdery mildew pathosystem. Plant Dis. 2010, 94, 339–344. [Google Scholar] [CrossRef] [PubMed]
  50. Wu, L.; McGrane, R.S.; Beattie, G.A. Light regulation of swarming motility in Pseudomonas syringae integrates signaling pathways mediated by a bacteriophytochrome and a LOV protein. mBio 2013, 4, e00334-13. [Google Scholar] [CrossRef] [PubMed]
  51. Alsanius, B.W.; Bergstrand, K.J.; Hartmann, R.; Gharaie, S.; Wohanka, W.; Dorais, M.; Rosberg, A.K. Ornamental flowers in new light: Artificial lighting shpares the microbial phyllosphere community structure of greenhouse grown sunflowers (Helianthus annuus L.). Sci. Hortic. 2017, 216, 234–247. [Google Scholar] [CrossRef]
  52. Alsanius, B.W.; Vaas, L.A.I.; Gharaie, S.; Karlsson, M.E.; Rosberg, A.K.; Grudén, M.; Wohanka, W.; Khalil, S.; Windstam, S. Dining in blue light impairs the appetite of some leaf epiphytes. Manuscript 2019. [Google Scholar]
  53. Gharaie, S.; Vaas, L.A.I.; Rosberg, A.K.; Windstam, S.T.; Karlsson, M.E.; Bergstrand, K.J.; Khalil, S.; Wohanka, W.; Alsanius, B.W. Light spectrum modifies the utilization pattern of energy sources in Pseudomonas sp. PLoS ONE 2017, 12, e0189862. [Google Scholar] [CrossRef] [PubMed]
  54. Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. The PRISMA Group, Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 2009, 6, e1000097. [Google Scholar] [CrossRef]
  55. Nelson, J.A.; Bugbee, B. Analysis of environmental effects on leaf temperature under sunlight, high pressure sodium and light emitting diodes. PLoS ONE 2015, 10, e0138930. [Google Scholar] [CrossRef] [PubMed]
  56. Hernández, R.; Kubota, C. Physiological responses of cucumber seedlings under different blue and red photon flux ratios using LEDs. Environ. Exp. Bot. 2014, 121, 66–74. [Google Scholar] [CrossRef]
  57. Bergstrand, K.J.; Schüssler, H.K. Growth, development and photosynthesis of some horticultural plants as affected by different supplementary lighting technologies. Eur. J. Hortic. Sci. 2013, 78, 119–125. [Google Scholar]
  58. Demotes-Mainard, S.; Péron, T.; Corot, A.; Bertheloot, J.; Le Gourriere, J.; Pelleschi-Travier, S.; Crespel, L.; Morel, P.; Huché-Thélier, L.; Boumaz, R.; et al. Plant responses to red and far-red lights, applications in horticulture. Environ. Exp. Bot. 2016, 121, 4–21. [Google Scholar] [CrossRef]
  59. Mortensen, L.M. The effect of photon flux density and lighting period on growth, flowering, powdery mildew and water relations of miniature roses. Am. J. Plant Sci. 2014, 5, 1813–1818. [Google Scholar] [CrossRef]
  60. O’Neill, T.M.; Shtienberg, D.; Elad, Y. Effect of some host and microclimate factors on infection of tomato stems by Botrytis cinerea. Plant Dis. 1997, 81, 36–40. [Google Scholar] [CrossRef] [PubMed]
  61. Kozai, T.; Niu, G.; Takagaki, M. (Eds.) Physical environmental factors and their properties. In Plant Factory: An Indoor Vertical Farming System for Efficient Quality Food Production; Elsevier Academic Press: Amsterdam, The Netherlands, 2016; pp. 129–140. [Google Scholar]
  62. Rünger, W. Licht und Temperatur im Zierpflanzenbau; Paul Parey: Berlin, Germany, 1964. [Google Scholar]
  63. Raviv, M.; Antignus, Y. UV radiation effects on pathogens and insect pests of greenhouse-grown crops. Photochem. Photobiol. 2004, 79, 219–226. [Google Scholar] [CrossRef] [PubMed]
  64. Von Zabeltitz, C. Cladding material. In Integrated Greenhouse Systems for Mild Climates; Springer: Heidelberg, Germany, 2011; pp. 145–167. [Google Scholar]
  65. Waaijenberg, D. Design, construction and maintenance of greenhouse structures. Acta Hortic. 2004, 710, 31–42. [Google Scholar] [CrossRef]
  66. Ballaré, C.L. Light regulation of plant defense. Ann. Rev. Plant Biol. 2014, 65, 335–363. [Google Scholar] [CrossRef] [PubMed]
  67. Clifford, S.C.; Runkle, E.S.; Langton, F.A.; Mead, A.; Foster, S.A.; Pearson, S.; Heins, R.D. Height control of poinsettia using photoselective filters. HortScience 2004, 39, 383–387. [Google Scholar] [CrossRef]
  68. Mata, D.A.; Botto, J.F. Manipulation of light environment to produce high-quality poinsettia plants. HortScience 2009, 44, 702–706. [Google Scholar] [CrossRef]
  69. McCree, K.J. The action spectrum, absorptance and quantum yield of photosynthesis in crop plants. Agric. Meteorol. 1972, 9, 191–216. [Google Scholar] [CrossRef]
  70. Massa, G.; Graham, T.; Haire, T.; Flemming, C.; Newsham, G.; Wheeler, R. Light-emitting diode light transmission through leaf tissue of seven different crops. HortScience 2015, 50, 501–506. [Google Scholar] [CrossRef]
  71. Bergstrand, K.J.; Mortensen, L.M.; Suthaparan, A.; Gislerød, H.R. Acclimatisation of greenhouse crops to differing light quality. Sci. Hortic. 2016, 204, 1–7. [Google Scholar] [CrossRef]
  72. Lin, K.H.; Huang, M.Y.; Huang, W.D.; Hsu, M.H.; Yang, Z.W.; Yang, C.M. The effects of red, blue, and white light-emitting diodes on the growth, development, and edible quality of hydroponically grown lettuce (Lactuca sativa L. var. capitata). Sci. Hortic. 2013, 150, 86–91. [Google Scholar] [CrossRef]
  73. Fankhauser, C.; Ulm, R. A photoreceptor’s on-off switch. Science 2016, 354, 282–283. [Google Scholar] [CrossRef] [PubMed]
  74. Folta, K.M.; Carvalho, S.D. Photoreceptors and control of horticultural plant traits. HortScience 2015, 50, 1274–1280. [Google Scholar] [CrossRef]
  75. Huché-Thélier, L.; Crespel, L.; Le Gourrierec, J.; Morel, P.; Sakr, S.; Leduc, N. Light signaling and plant responses to blue light and UV radiation—Perspectives for applications in horticulture. Environ. Exp. Bot. 2016, 121, 22–38. [Google Scholar] [CrossRef]
  76. Lercari, B.; Bretzel, F.; Piazza, S. Effects of UV Treatments on Stem Growth of Some Greenhouse Crops. Act Hortic. 1992, 327, 99–104. [Google Scholar] [CrossRef]
  77. Abidi, F.; Girault, T.; Douillet, O.; Guillemain, G.; Sintes, G.; Laffaire, M.; Ahmed, H.B.; Smiti, S.; Huché-Thélier, L.; Leduc, N. Blue light effects on rose photosynthesis and photomorphogenesis. Plant Biol. 2013, 15, 67–74. [Google Scholar] [CrossRef]
  78. Glowacka, B. The effect of blue light on the height and habit of the tomato (Lycopersicon esculentum Mill.) transplant. Folia Hortic. 2004, 16, 3–10. [Google Scholar]
  79. Piszczek, P.; Głowacka, B. Effect of the colour of light on cucumber (Cucumis sativus L.) seedlings. Veg. Crop. Res. Bull. 2008, 68, 71–80. [Google Scholar] [CrossRef]
  80. Terfa, M.T.; Roro, A.G.; Olsen, J.E.; Torre, S. Effects of UV radiation on growth and postharvest characteristics of three pot rose cultivars grown at different altitudes. Sci. Hortic. 2014, 178, 184–191. [Google Scholar] [CrossRef]
  81. Torre, S.; Roro, A.G.; Bengtsson, S.; Mortensen, L.; Solhaug, K.A.; Gislerød, H.R.; Olsen, J.E. Control of plant morphology by UV-B and UV-B-temperature interactions. Acta Hortic. 2012, 956, 207–214. [Google Scholar] [CrossRef]
  82. Islam, M.A.; Kuwar, G.; Clarke, J.L.; Blystad, D.R.; Gislerød, H.R.; Olsen, J.E.; Torre, S. Artificial light from light emitting diodes (LEDs) with a high portion of blue light results in shorter poinsettias compared to high pressure sodium (HPS) lamps. Sci. Hortic. 2012, 147, 136–143. [Google Scholar] [CrossRef]
  83. Brown, C.S.; Schuerger, A.C.; Sager, J.C. Growth and photomorphogenesis of pepper plants under red light-emitting diodes with supplemental blue or far-red lighting. J. Am. Soc. Hortic. Sci. 1995, 120, 808–813. [Google Scholar] [CrossRef] [PubMed]
  84. Ohashi-Kaneko, K.; Takase, M.; Kon, N.; Fujiwara, K.; Kurata, K. Effect of light quality on growth and vegetable quality in leaf lettuce, spinach and komatsuna. Environ. Control Biol. 2007, 45, 189–198. [Google Scholar] [CrossRef]
  85. Wargent, J.J.; Taylor, A.; Paul, N.D. UV supplementation for growth and disease control. Acta Hortic. 2006, 711, 333–338. [Google Scholar] [CrossRef]
  86. Hogewoning, S.W.; Trouwborst, G.; Maljaars, H.; Poorter, H.; van Ieperen, W.; Harbinson, J. Blue light dose–responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue light. J. Exp. Bot. 2010, 61, 3107–3117. [Google Scholar] [CrossRef]
  87. O’Carrigan, A.; Babla, M.; Wang, F.; Liu, X.; Mak, M.; Thomas, R.; Bellotti, B.; Chen, Z.H. Analysis of gas exchange, stomatal behaviour and micronutrients uncovers dynamic response and adaptation of tomato plants to monochromatic light treatments. Plant Physiol. Biochem. 2014, 82, 105–115. [Google Scholar] [CrossRef]
  88. Lee, J.S.; Lee, C.A.; Kim, Y.H.; Yun, S.J. Shorter wavelength blue light promotes growth of green perilla (Perilla frutescens). Int. J. Agric. Biol. 2014, 16, 1177–1182. [Google Scholar]
  89. Nanya, K.; Ishigami, Y.; Hikosaka, S.; Goto, E. Effects of blue and red light on stem elongation and flowering of tomato seedlings. Acta Hortic. 2012, 956, 261–266. [Google Scholar] [CrossRef]
  90. Hogewoning, S.W.; Trouwborst, G.; Meinen, E.; van Ieperen, W. Finding the optimal growth-light spectrum for greenhouse crops. Acta Hortic. 2012, 956, 357–363. [Google Scholar] [CrossRef]
  91. Young, H.M.; George, S.; Narváez, D.F.; Srivastava, P.; Schuerger, A.C.; Wright, D.L.; Marois, J.J. Effect of solar radiation on severity of soybean rust. Phytopathology 2012, 102, 794–803. [Google Scholar] [CrossRef] [PubMed]
  92. Yamasaki, S.; Noguchi, N.; Mimaki, K. Continuous UV-B irradiation induces morphological changes and the accumulation of polyphenolic compounds on the surface of cucumber cotyledons. J. Radiat. Res. 2007, 48, 443–454. [Google Scholar] [CrossRef] [PubMed]
  93. Casal, J.J.; Smith, H. The function, action and adaptive significance of phytochrome in light-grown plants. Plant Cell Environ. 1989, 12, 855–862. [Google Scholar] [CrossRef]
  94. Li, Q.; Kubota, C. Effects of supplemental light quality on growth and phytochemicals of baby leaf lettuce. Environ. Exp. Bot. 2009, 67, 59–64. [Google Scholar] [CrossRef]
  95. Craig, D.; Runkle, E.S. Using leds to quantify the effect of the red to far-red ratio of night-interruption lighting on flowering of photoperiodic crops. Acta Hortic. 2012, 956, 179–185. [Google Scholar] [CrossRef]
  96. Solymosi, K.; Schoefs, B. Etioplast and etio-chloroplast formation under natural conditions: The dark side of chlorophyll biosynthesis in angiosperms. Photosynth. Res. 2010, 105, 143–166. [Google Scholar] [CrossRef]
  97. Niyogi, K.K. Photoprotection revisited: Genetic and molecular approaches. Ann. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 33. [Google Scholar] [CrossRef]
  98. Wang, X.Y.; Xu, X.M.; Cui, J. The importance of blue light for leaf area expansion, development of photosynthetic apparatus, and chloroplast ultrastructure of Cucumis sativus grown under weak light. Photosynthetica 2015, 53, 1–10. [Google Scholar] [CrossRef]
  99. Lefsrud, M.G.; Kopsell, D.A.; Sams, C.E. Irradiance from distinct wave length light-emitting diodes affect secondary metabolites in kale. HortScience 2008, 43, 2243–2244. [Google Scholar] [CrossRef]
  100. Hoffmann, A.M.; Noga, G.; Hunsche, M. High blue light improves acclimation and photosynthetic recovery of pepper plants exposed to UV stress. Environ. Exp. Bot. 2015, 109, 254–263. [Google Scholar] [CrossRef]
  101. Li, J.; Hikosaka, S.; Goto, E. Effects of light quality and photosynthetic photon flux on growth and carotenoid pigments in spinach (Spinacia oleracea L.). Acta Hortic. 2009, 907, 105–110. [Google Scholar] [CrossRef]
  102. Lidon, F.J.C.; Reboredo, F.H.; Leitão, A.E.; Silva, M.M.A.; Duarte, M.P.; Ramalho, J.C. Impact of UV-B radiation on photosynthesis—An overview. Emir. J. Food Agric. 2012, 24, 546–556. [Google Scholar] [CrossRef]
  103. Naznin, M.T.; Lefsrud, M.; Gagne, J.D.; Schwalb, M.; Bissonnette, B.H. Different wavelengths of LED light affect on plant photosynthesis. HortScience 2012, 47, S191. [Google Scholar]
  104. Opdam, J.G.; Schoonderbeek, G.G.; Heller, E.B.; Gelder, A. Closed green-house: A starting point for sustainable entrepreneurship in horticulture. Acta Hortic. 2005, 691, 517–524. [Google Scholar] [CrossRef]
  105. Trouwborst, G.; Hogewoning, S.W.; van Kooten, O.; Harbinson, J.; van Ieperen, W. Plasticity of photosynthesis after the ‘red light syndrome’ in cucumber. Environ. Exp. Bot. 2016, 121, 75–82. [Google Scholar] [CrossRef]
  106. Bian, Z.H.; Yang, Q.C.; Liu, W.K. Effects of light quality on the accumulation of phytochemicals in vegetables produced in controlled environments: A review. J. Sci. Food Agric. 2015, 95, 869–877. [Google Scholar] [CrossRef]
  107. Samuolienè, G.; Viršilè, A.; Brazaitytè, A.; Jankauskienè, J.; Duchovskis, P.; Novickovas, A. Effect of supplementary pre-harvest LED lighting on the antioxidant and nutritional properties of green vegetables. Acta Hortic. 2010, 939, 85–91. [Google Scholar] [CrossRef]
  108. Britz, S.J.; Sager, J.C. Photomorphogenesis and photoassimilation in soybean and sorghum grown under broad spectrum or blue-deficient light sources. Plant Physiol. 1990, 94, 448–454. [Google Scholar] [CrossRef]
  109. Johkan, M.; Shoji, K.; Goto, F.; Hashida, S.; Yoshihara, T. Blue light-emitting diode light irradiation of seedlings improves seedling quality and growth after transplanting in red leaf lettuce. HortScience 2010, 45, 1809–1814. [Google Scholar] [CrossRef]
  110. Kim, K.; Kook, H.S.; Jang, Y.J.; Lee, W.H.; Kamala-Kannan, S.; Chae, J.C.; Lee, K.J. The effect of blue-light emitting diodes on antioxidant properties and resistance to Botrytis cinerea in tomato. J. Plant Pathol. Microbiol. 2013, 4, 203. [Google Scholar] [CrossRef]
  111. Li, H.M.; Tang, C.M.; Xu, Z.G.; Liu, X.Y.; Han, X.L. Effects of different light sources on the growth of non-heading Chinese cabbage (Brassica campestris L.). J. Agric. Sci. 2012, 4, 262–273. [Google Scholar] [CrossRef]
  112. Li, H.M.; Xu, Z.G.; Tang, C.M. Effect of light-emitting diodes on growth and morphogenesis of upland cotton (Gossypium hirsutum L.) plantlets in vitro. Plant Cell Tissue Organ Cult. 2010, 103, 155–163. [Google Scholar] [CrossRef]
  113. Soebo, A.; Krekling, T.; Applegren, M. Light quality affects photosynthesis and leaf anatomy of birch plantlets in vitro. Plant Cell Tissue Organ Cult. 1995, 41, 177–185. [Google Scholar] [CrossRef]
  114. Knief, C.; Delmotte, N.; Chaffron, S.; Stark, M.; Innerebner, G.; Wassmann, R.; von Mering, C.; Vorholt, J.A. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 2012, 6, 1378–1390. [Google Scholar] [CrossRef] [PubMed]
  115. Bantis, F.; Ouzounis, T.; Radoglou, K. Artificial LED lighting enhances growth characteristics and total phenolic content of Ocimum basilicum, but variably affects transplant success. Sci. Hortic. 2016, 198, 277–283. [Google Scholar] [CrossRef]
  116. Samuolienè, G.; Sirtautas, R.; Brazaitytè, A.; Duchovskis, P. LED lighting and seasonality effects antioxidant properties of baby leaf lettuce. Food Chem. 2012, 134, 1494–1499. [Google Scholar] [CrossRef]
  117. Chen, W.H.; Xu, Z.G.; Liu, X.Y.; Yang, Y.; Wang, Z.H.M.; Song, F.F. Effect of LED light source on the growth and quality of different lettuce varieties. Acta Bot. Boreali Occident. Sin. 2011, 31, 1434–1440. [Google Scholar]
  118. Liu, W.K.; Yang, Q.C. Effects of supplemental UV-A and UV-C irradiation on growth, photosynthetic pigments and nutritional quality of pea seedlings. Acta Hortic. 2012, 956, 657–663. [Google Scholar] [CrossRef]
  119. Mizuno, T.; Amaki, W.; Watanabe, H. Effects of monochromatic light irradiation by LED on the growth and anthocyanin contents in leaves of cabbage seedlings. Acta Hortic. 2009, 907, 179–184. [Google Scholar] [CrossRef]
  120. Zhang, T.; Folta, K.M. Green light signaling and adaptive response. Plant Signal Behav. 2012, 7, 75–78. [Google Scholar] [CrossRef]
  121. Kopsell, D.A.; Sams, C.E. Increases in shoot tissue pigments, glucosinolates, and mineral elements in sprouting broccoli after exposure to short-duration blue light from light-emitting diodes. J. Am. Soc. Hortic. Sci. 2013, 138, 31–37. [Google Scholar] [CrossRef]
  122. Kopsell, D.A.; Sams, C.E.; Barickman, T.C.; Morrow, R.C. Sprouting broccoli accumulate higher concentrations of nutritionally important metabolites under narrow-band light-emitting diode lighting. J. Am. Soc. Hortic. Sci. 2014, 139, 469–477. [Google Scholar] [CrossRef]
  123. Zukalova, H.; Vasak, J.; Nerad, D.; Stranc, P. The role of glucosinolates of Brassica genus in the crop system. Rostlinna Výroba 2002, 48, 181–189. [Google Scholar] [CrossRef]
  124. Colquhoun, T.A.; Schwieterman, M.L.; Gilbert, J.L.; Jaworski, E.A.; Langer, K.M.; Jones, C.R.; Rushing, G.V.; Hunter, T.M.; Olmstead, J.; Clark, D.G.; et al. Light modulation of volatile organic compounds from petunia flowers and select fruits. Postharvest Biol. Technol. 2013, 86, 37–44. [Google Scholar] [CrossRef]
  125. Vänninen, I.; Pinto, D.M.; Nissinen, A.I.; Johansen, N.S.; Shipp, L. In the light of new greenhouse technologies: 1. Plant-mediated effects of artificial lighting on arthropods and tritrophic interactions. Ann. Appl. Biol. 2010, 157, 393–414. [Google Scholar] [CrossRef]
  126. Wu, L.; Yang, H.Q. Cryptochrome 1 is implicated in promoting R protein- mediated plant resistance to Pseudomonas syringae in Arabidopsis. Mol. Plant 2010, 3, 539–548. [Google Scholar] [CrossRef] [PubMed]
  127. Wang, H.; Jiang, Y.P.; Yu, H.J.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Yu, J.Q. Light quality affects incidence of powdery mildew, expression of defence-related genes and associated metabolism in cucumber plants. Eur. J. Plant Pathol. 2010, 127, 125–135. [Google Scholar] [CrossRef]
  128. Shibuya, T.; Itagaki, K.; Tojo, M.; Endo, R.; Kitaya, Y. Fluorescent illumination with high red-to-far-red ratio improves resistance of cucumber seedlings to powdery mildew. HortScience 2011, 46, 429–431. [Google Scholar] [CrossRef]
  129. Cargnel, M.D.; Demkura, P.V.; Ballare, C.L. Linking phytochrome to plant immunity: Low red: Far-red ratios increase Arabidopsis susceptibility to Botrytis cinerea by reducing the biosynthesis of indolic glucosinolates and camalexin. New Phytol. 2014, 204, 342–354. [Google Scholar] [CrossRef] [PubMed]
  130. De Wit, M.; Spoel, S.H.; Sanchez-Perez, G.F.; Gommers, C.M.M.; Pieterse, C.M.J.; Voesenek, L.; Pierik, R. Perception of low red:far-red ratio compromises both salicylic acid- and jasmonic acid-dependent pathogen defences in Arabidopsis. Plant J. 2013, 75, 90–103. [Google Scholar] [CrossRef] [PubMed]
  131. Moreno, J.E.; Tao, Y.; Chory, J.; Ballare, C.L. Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc. Natl. Acad. Sci. USA 2009, 106, 4935–4940. [Google Scholar] [CrossRef] [PubMed]
  132. Kurepin, L.V.; Emery, R.J.N.; Pharis, R.P.; Reid, D.M. Uncoupling light quality from light irradiance effects in Helianthus annuus shoots: Putative roles for plant hormones in leaf and internode growth. J. Exp. Bot. 2007, 58, 2145–2157. [Google Scholar] [CrossRef] [PubMed]
  133. Lee, M.K.; Arasu, M.V.; Park, S.; Byeon, D.H.; Chung, S.O.; Park, S.U.; Lim, Y.P.; Kim, S.J. LED lights enhance metabolites and antioxidants in chinese cabbage and kale. Braz. Arch. Biol. Technol. 2016, 59, e16150546. [Google Scholar] [CrossRef]
  134. Muneer, S.; Kim, E.J.; Park, J.S.; Lee, J.H. Influence of green, red and blue light emitting diodes on multiprotein complex proteins and photosynthetic activity under different light intensities in lettuce leaves (Lactuca sativa L.). Int. J. Mol. Sci. 2014, 15, 4657–4670. [Google Scholar] [CrossRef] [PubMed]
  135. Naznin, M.T.; Lefsrud, M.; Gravel, V.; Hao, X. Different ratios of red and blue LEDs light affect on coriander productivity and antioxidant properties. Acta Hortic. 2016, 1134, 223–229. [Google Scholar] [CrossRef]
  136. Wu, M.C.; Hou, C.Y.; Jiang, C.M.; Wang, Y.T.; Wang, C.Y.; Chen, H.H.; Chang, H.M. A novel approach of LED light radiation improves the antioxidant activity of pea seedlings. Food Chem. 2007, 101, 1753–1758. [Google Scholar] [CrossRef]
  137. Chen, L.; Zhao, F.; Zhang, M.; Hong-Hui, L.; Xi, D.H. Effects of light quality on the interaction between cucumber mosaic virus and Nicotiana tabacum. J. Phytopathol. 2015, 163, 1002–1013. [Google Scholar] [CrossRef]
  138. Xu, H.; Fu, Y.; Li, T.; Wang, R. Effects of different LED light wavelengths on the resistance of tomato against Botrytis cinerea and the corresponding physiological mechanisms. J. Integr. Agric. 2017, 16, 106–114. [Google Scholar] [CrossRef]
  139. Bavaresco, L.; Fregoni, C.; van Zeller de Macedo Basto Gonçalves, M.I.; Vezzulli, S. Physiology and molecular biology of grapevine stilbenes—An update. In Grapevine Molecular Physiology & Biotechnology, 2nd ed.; Roubelakis-Angelakis, K.A., Ed.; Springer Science and Business Media B.V.: Amsterdam, The Netherlands; New York, NY, USA, 2009; pp. 341–364. [Google Scholar]
  140. Ahn, S.Y.; Kim, S.A.; Choi, S.J.; Yun, H.K. Comparison of accumulation of stilbene compounds and stilbene related gene expression in two grape berries irradiated with different light sources. Hortic. Environ. Biotechnol. 2015, 56, 36–43. [Google Scholar] [CrossRef]
  141. Jeandet, P.; Douillt-Breuil, A.C.; Bessis, R.; Debord, S.; Sbaghi, M.; Adrian, M. Phytoalexins from the vitaceae: Biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J. Agric. Food Chem. 2002, 50, 2731–2741. [Google Scholar] [CrossRef]
  142. Parada, R.Y.; Mon-nai, W.; Ueno, M.; Kihara, J.; Arase, S. Red-light-induced resistance to brown spot disease caused by Bipolaris oryzae in rice. J. Phytopathol. 2014, 163, 116–123. [Google Scholar] [CrossRef]
  143. Balint-Kurti, P.; Simmons, S.J.; Blum, J.E.; Ballaré, C.L.; Stapleton, A.E. Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol. Plant Microbe Interact. 2010, 23, 473–484. [Google Scholar] [CrossRef] [PubMed]
  144. Aruscavage, D.; Phelan, P.L.; Lee, K.; LeJeune, J.T. Impact of changes in sugar exudate created by biological damage to tomato plants on the persistence of Escherichia coli O157:H7. J. Food Sci. 2010, 75, M187–M192. [Google Scholar] [CrossRef] [PubMed]
  145. 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 2001, 98, 3446–3453. [Google Scholar] [CrossRef] [PubMed]
  146. Aschenbrenner, A.K.; Amrehn, E.; Bechtel, L.; Spring, O. Trichome differentiation on leaf primordia of Helianthus annuus (Asteraceae): Morphology, gene expression and metabolite profile. Planta 2015, 41, 837–846. [Google Scholar] [CrossRef]
  147. Aschenbrenner, A.K.; Horakh, S.; Spring, O. Linear glandular trichomes of Helianthus (Asteraceae): Morphology, localization, metabolite activity and occurrence. AoB Plants 2013, 5. [Google Scholar] [CrossRef]
  148. Huang, S.S.; Kirchoff, B.K.; Liao, J.P. The capitate and peltate glandular trichomes of Lavandula pinnata L. (Lamiaceae): Histochemistry, ultrastructure, and secretion. J. Torrey Bot. Soc. 2008, 135, 155–167. [Google Scholar] [CrossRef]
  149. 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. 2008, 21, 269–282. [Google Scholar] [CrossRef]
  150. 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. 2007, 20, 1512–1522. [Google Scholar] [CrossRef]
  151. Nagendran, R.; Lee, Y.H. Green and red light reduces the disease severity by Pseudomonas cichorii JBC1 in tomato plants via upregulation of defense-related gene expression. Phytopathology 2015, 105, 412–418. [Google Scholar] [CrossRef]
  152. Islam, S.Z.; Babadoost, M.; Bekal, S.; Lambert, K. Red light-induced systemic disease resistance against root-knot nematode Meloidogyne javanica and Pseudomonas syringae pv. tomato DC 3000. J. Phytopathol. 2008, 156, 708–714. [Google Scholar] [CrossRef]
  153. Yadav, R.K.P.; Karamanoli, K.; Vokou, D. Bacterial colonization of the phyllosphere of Mediterranean perennial species as influenced by leaf structural and chemical features. Microb. Ecol. 2005, 50, 185–196. [Google Scholar] [CrossRef] [PubMed]
  154. Gratani, L.; Covone, F.; Larcher, W. Leaf plasticity in response to light of three evergreen species of the Mediterranean maquis. Trees 2006, 20, 549–558. [Google Scholar] [CrossRef]
  155. Steinmüller, D.; Tevini, M. Action of ultraviolet radiation (UV-B) upon cuticular waxes in some crop plants. Planta 1985, 164, 557–564. [Google Scholar] [CrossRef] [PubMed]
  156. Garrett, T.R.; Bhakoo, M.; Zhang, Z. Bacterial adhesion and biofilms on surfaces. Prog. Nat. Sci. 2008, 18, 1049–1056. [Google Scholar] [CrossRef]
  157. Gomelsky, M.; Hoff, W.D. Light helps bacteria make important lifestyle decisions. Trends Microbiol. 2011, 19, 441–448. [Google Scholar] [CrossRef] [PubMed]
  158. Losi, A.; Gärtner, W. Bacterial bilin- and flavin-binding photoreceptors. Photochem. Photobiol. Sci. 2008, 7, 1168–1178. [Google Scholar] [CrossRef]
  159. Pertot, I.; Fiamingo, F.; Amsalem, L.; Maymon, M.; Freeman, S.; Gobbin, D.; Elad, Y. Sensitivity of two Podosphaera aphanis populations to disease control agents. J. Plant Pathol. 2007, 89, 85–96. [Google Scholar]
  160. Xiao, C.; Chandler, C.; Price, J.; Duval, J.; Mertely, J.; Legard, D. Comparison of epidemics of Botrytis fruit rot and powdery mildew of strawberry in large plastic tunnel and field production systems. Plant Dis. 2001, 85, 901–909. [Google Scholar] [CrossRef]
  161. Kraiselburd, I.; Alet, A.I.; Tondo, M.L.; Petrocelli, S.; Daurelio, L.D.; Monzón, J.; Ruiz, O.A.; Losi, A.; Orellano, E.G. A LOV protein modulates the physiological attributes of Xanthomonas axonopodis pv. citri relevant for host plant colonization. PLoS ONE 2012, 7, e38226. [Google Scholar] [CrossRef]
  162. Mao, D.; Tao, J.; Li, C.; Luo, C.; Zheng, L.; He, C. Light signalling mediated by Per-ARNT-Sim domain-containing proteins in Xanthomonas campestris pv. campestris. FEMS Microbiol. Lett. 2012, 326, 31–39. [Google Scholar] [CrossRef] [PubMed]
  163. Müller, G.L.; Tuttobene, M.; Altilio, M.; Martínez Amezaga, M.; Nguyen, M.; Cribb, P.; Cybulski, L.E.; Ramírez, M.S.; Altabe, S.; Mussi, M.A. Light modulates metabolic pathways and other novel physiological traits in the human pathogen Acinetobacter baumannii. J. Bacteriol. 2017, 199, e00011-17. [Google Scholar] [CrossRef] [PubMed]
  164. Yu, S.M.; Lee, Y.H. Effect of light quality on Bacillus amyloliquefaciens JBC36 and its biocontrol efficacy. Biol. Control 2013, 64, 203–210. [Google Scholar] [CrossRef]
  165. Imada, K.; Tanaka, S.; Ibaraki, Y.; Yoshimura, K.; Ito, S. Antifungal effect of 405-nm light on Botrytis cinerea. Lett. Appl. Microbiol. 2014, 59, 670–676. [Google Scholar] [CrossRef] [PubMed]
  166. Wilde, A.; Mullineaux, C.W. Light-controlled motility in prokaryotes and the problem of directional light perception. FEMS Microbiol. Rev. 2017, 41, 900–922. [Google Scholar] [CrossRef] [PubMed]
  167. Rajalingam, N.; Lee, J.H. Effects of green light on the gene expression and virulence of the plant pathogen Pseudomonas cichorii JBC1. Eur. J. Plant Pathol. 2018, 150, 223–236. [Google Scholar] [CrossRef]
  168. Someya, N.; Nakajima, M.; Hamamoto, H.; Yamaguchi, I.; Akutsu, K. Effects of light conditions on prodigiosin stability in the biocontrol bacterium Serratia marcescens strain B2. J. Gen. Plant Pathol. 2004, 70, 367–370. [Google Scholar] [CrossRef]
  169. Guffy, J.S.; Wilborn, J. In vitro bactericidal effects of 405-nm and 470-nm blue light. Photobiomodulation Photomed. Laser Surg. 2006, 24, 684–688. [Google Scholar] [CrossRef]
  170. Berrocal-Tito, G.; Sametz-Baron, L.; Eichenberg, K.; Horwitz, B.A.; Herrera-Estrella, A. Rapid blue light regulation of a Trichoderma harzianum photolyase gene. J. Biol. Chem. 1999, 274, 14288–14294. [Google Scholar] [CrossRef]
  171. Papavizas, G.C. Trichoderma and Gliocladium: Biology, ecology and potential for biocontrol. Ann. Rev. Phytopathol. 1985, 23, 23–54. [Google Scholar] [CrossRef]
  172. Van der Horst, M.A.; Hellingwerf, K.J. Photoreceptor proteins, “star actors of modern times”: A review of the functional dynamics in the structure of representative members of six different photoreceptor families. Acc. Chem. Res. 2004, 37, 13–20. [Google Scholar] [CrossRef] [PubMed]
  173. Van der Horst, M.A.; Key, J.; Hellingwerf, K.J. Photosensing in chemotrophic, non-phototrophic bacteria: Let there be light sensing too. Trends Microbiol. 2007, 15, 554–562. [Google Scholar] [CrossRef] [PubMed]
  174. Jenal, U.; Malone, J. Mechanisms of Cyclic-di-GMP signaling in bacteria. Ann. Rev. Genet. 2006, 40, 385–407. [Google Scholar] [CrossRef] [PubMed]
  175. Hengge, R.; Galperin, M.Y.; Ghigo, J.M.; Gomelsky, M.; Green, J.; Hughes, K.T.; Jenal, U.; Landini, P. Systematic Nomenclature for GGDEF and EAL Domain-Containing Cyclic Di-GMP Turnover Proteins of Escherichia coli. J. Bacteriol. 2016, 198, 7–11. [Google Scholar] [CrossRef]
  176. Bumah, V.V.; Masson-Meyers, D.S.; Cashin, S.; Enwemeka, C.S. Optimization of the antimicrobial effect of blue light on methicillin-resistant Staphylococcus aureus (MRSA) in vitro. Lasers Surg. Med. 2015, 47, 266–272. [Google Scholar] [CrossRef] [PubMed]
  177. Halstead, F.D.; Thwaite, J.E.; Burt, R.; Laws, T.R.; Raguse, M.; Moeller, R.; Webber, M.A.; Oppenheim, B.A. Antibacterial activity of blue light against nosocomial wound pathogens growing planktonically and as mature biofilms. Appl. Environ. Microbiol. 2016, 82, 4006–4016. [Google Scholar] [CrossRef] [PubMed]
  178. Glantz, S.T.; Carpenter, E.J.; Melkonian, M.; Gardner, K.H.; Boyden, E.S.; Wong, G.K.S.; Chow, B.Y. Functional and topological diversity of LOV domain photoreceptors. Proc. Natl. Acad. Sci. USA 2016, 113, E1442–E1451. [Google Scholar] [CrossRef]
  179. Zayner, J.P.; Antoniou, C.; French, A.R.; Hause, R.J., Jr.; Sosnick, T.R. Investigating models of protein function and allostery with a widespread mutational analysis of a light-activated protein. Biophys. J. 2013, 105, 1027–1036. [Google Scholar] [CrossRef]
  180. Kraiselburd, I.; Moyano, L.; Carrau, A.; Tano, J.; Orellano, E.G. Bacterial photosensory proteins and their role in plant–pathogen interactions. Photochem. Photobiol. 2017, 93, 666–674. [Google Scholar] [CrossRef]
  181. Masuda, S. Light detection and signal transduction in the BLUF photoreceptors. Plant Cell Physiol. 2013, 54, 171–179. [Google Scholar] [CrossRef]
  182. Tschowri, N.; Busse, S.; Hengge, R. The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue-light response of Escherichia coli. Genes Dev. 2009, 23, 522–534. [Google Scholar] [CrossRef] [PubMed]
  183. Meyer, T.E.; Yakali, E.; Cusanovich, M.A.; Tollin, F. Properties of a water soluble yellow protein isolated from a halophilic phototrophic bacterium that has photochemical activity analogous to sensory rhodopsin. Biochemistry 1987, 26, 418–423. [Google Scholar] [CrossRef] [PubMed]
  184. Meyer, T.E.; Kyndt, J.A.; Memmi, S.; Moser, T.; Colon-Acevedo, B.; Devreese, B.; Van Beeumen, J. The growing family of photoactive yellow proteins and their presumed functional roles. Photochem. Photobiol. Sci. 2012, 11, 1495–1514. [Google Scholar] [CrossRef] [PubMed]
  185. Imamoto, Y.; Kataoka, M. Structure and Photoreaction of Photoactive Yellow Protein, a Structural Prototype of the PAS Domain Superfamily†. Photochem. Photobiol. 2007, 83, 40–49. [Google Scholar] [CrossRef] [PubMed]
  186. Nielsen, I.B.; Boyé-Péronne, S.; El Ghazaly, M.O.A.; Kristensen, M.B.; Brøndsted Nielsen, S.; Andersen, L.H. Absorption spectra of photoactive yellow protein chromophores in vacuum. Biophys. J. 2005, 89, 2597–2604. [Google Scholar] [CrossRef] [PubMed]
  187. Hawkes, C.V.; Connor, E.W. Translating phytobiomes from theory to practice: Ecological and evolutionary considerations. Phytobiomes 2017, 1, 57–69. [Google Scholar] [CrossRef]
  188. Werner, G.D.A.; Strassmann, J.E.; Ivens, A.B.F.; Engelmoor, D.J.P.; Verbryggen, E.; Queller, D.C.; Roë, R.; Collins Johnson, N.; Hammerstein, P.; Kiers, E.T. Evolution of microbial markets. Proc. Natl. Acad. Sci. USA 2014, 111, 1237–1244. [Google Scholar] [CrossRef]
  189. Mercier, J.; Lindow, S.E. Role of leaf surface sugars in colonization of plants by bacterial epiphytes. Appl. Environ. Microbiol. 2000, 66, 369–374. [Google Scholar] [CrossRef]
  190. Tukey, H.B.J.; Morgan, J.V. Injury to foliage and its effect upon the leaching of nutrients from above-ground plant parts. Physiol. Plant. 1963, 16, 557–564. [Google Scholar] [CrossRef]
Figure 1. Most important growth parameters affecting the phyllosphere of greenhouse crops. (Illustration: M. Dorais).
Figure 1. Most important growth parameters affecting the phyllosphere of greenhouse crops. (Illustration: M. Dorais).
Horticulturae 05 00041 g001
Figure 2. Bacterial phyllosphere community structure of some greenhouse crops artificially illuminated with high-pressure sodium lamps (HPS). Blue: sunflower, Helianthus annuus L. [51]. Orange: baby leaf spinach (Spinacia oleacea); grey: rocket (Diplotaxis tenuifolia) [Alsanius, unpublished data]. (Illustration: B. Alsanius).
Figure 2. Bacterial phyllosphere community structure of some greenhouse crops artificially illuminated with high-pressure sodium lamps (HPS). Blue: sunflower, Helianthus annuus L. [51]. Orange: baby leaf spinach (Spinacia oleacea); grey: rocket (Diplotaxis tenuifolia) [Alsanius, unpublished data]. (Illustration: B. Alsanius).
Horticulturae 05 00041 g002
Figure 3. Plant processes affected by light that can be targeted to promote beneficial phyllosphere components, contributing to greenhouse crop productivity. (Illustration: M. Dorais).
Figure 3. Plant processes affected by light that can be targeted to promote beneficial phyllosphere components, contributing to greenhouse crop productivity. (Illustration: M. Dorais).
Horticulturae 05 00041 g003
Table 1. Commonly used sources for artificial assimilation lighting (high-pressure sodium, HPS; metal halide; light tube; continuous spectrum polychromatic light-emitting diode (LED). Parameters of importance for plant–microbe interactions are displayed (ultraviolet light, UV; photosynthetically active radiation, PAR). Heat emissions directed towards (↓) or away from (↑) the crop are indicated by arrows.
Table 1. Commonly used sources for artificial assimilation lighting (high-pressure sodium, HPS; metal halide; light tube; continuous spectrum polychromatic light-emitting diode (LED). Parameters of importance for plant–microbe interactions are displayed (ultraviolet light, UV; photosynthetically active radiation, PAR). Heat emissions directed towards (↓) or away from (↑) the crop are indicated by arrows.
Lamp TypeEffect (W)Infra-RedUVPAR 1Direction of Heat EmissionsReferences
HPS 2400HighLow1.6[41]
Metal halide 3400HighLown/a[42]
Light tube 458MediumLown/a
LED 1 5630NoneNone1.85[43]
LED 2 6550NoneNone2.5[44]
LED 3 7400NoneNone2.3[45]
1 Spectral distribution for different lamp types shown in Figure S1. 2 Philips Master, Philips, Eidhoven, the Netherlands; 3 Philips Master HPI-T plus; Philips, Eindhoven, the Netherlands. 4 Osram G13 T8 58W 840, Osram, Munich, Germany; 5 Heliospectra EOS, Heliospectra AB, Gothenburg, Sweden; 6 Senmatic FL300 Grow, Senmatic A/S, Soendersoe, Denmark; 7 Valoya RX400, Valoya Oy, Helsinki, Finland.
Table 2. Summary of different microorganisms, the photoreceptor/s they contain, and the physiological response to different light spectra.
Table 2. Summary of different microorganisms, the photoreceptor/s they contain, and the physiological response to different light spectra.
OrganismLight QualityWave Length (nm)PhotoreceptorPhotoreceptor ArchitectureEffectRef.
Acinetobacter baumanniiBlue415BLUF, LOVEAL-GAF-GGDEF-LOV-GGDEFBiofilm formation, metabolism, virulence[163]
Bacillus amylolique-faciensRed
LOVLOV-STASSwarming motility, biofilm formation, antifungal activity[164]
Botrytis cinereaBlue405PHY, LOVPAS-GAF-PHY-HK
LOV-PAS, short LOV
Inhibited mycelial growth, virulence[165]
Pseudomonas aeringiunosaBlue405PHY, LOVPAS-GAF-PHY-kinase
Short LOV
Survival, virulence factors[166]
P. cichoriiGreenNILOVHATP-HisKA-LOV-RRSiderophore and phytotoxic lipopeptide production[167]
P. syringaeRed/Far-red
Short LOV
Decreased swarming motility[50]
Podosphaera pannosaBlue420–520 Reduced germination and conidia formation [49]
Serratia marcescensBlue
470 Antibiotic production[168]
Sphaerotheca fuligineaRedNI 1 Disease suppression[127]
Staphylococcus aureusBlue405, 470 Growth[169]
Trichoderma harzianumBlueNI Induced gene expression of phr1[170]
Xanthomonas axonopodisLight/
Motility, adhesion, biofilm formation[161]
Xanthomonas campestrisRed/
Growth, motility[162]
1 NI = not indicated.
Table 3. Ecological theories and principles of interest to use in light-assisted phyllosphere studies.
Table 3. Ecological theories and principles of interest to use in light-assisted phyllosphere studies.
Theory/PrinciplesModes of ActionPotential Research QuestionsLight Spectra of Interest
Niche theory
Priority effectsPre-emptying of space and resources by the first arriving speciesHeterotrophic utilization of leaf lysates/organic compounds and their impact on secondary metabolitesB 1, G 2, Y 3, R 4, R:FR 5
Competitive dominanceDominance due to efficient resource use under prevailing stable conditions
Niche partitioningCoexistenceLight-quality-associated impact on biofilm community structure
Bacterial–fungi symbionts/Suitable microbe combination
Plant–microbe and microbe–microbe compatibility
B, G, Y, R, R:FR
Storage effectCoexistence of microbes within the same ecological community Storage effects in non-phototrophic non-spore-forming bacterial leaf colonizersB, G, Y, R, R:FR
Niche modificationInvasion of leaf interiorLight quality as a driver towards an endophytic lifestyleB, G, Y, R, R:FR
Biofilm formationLight quality as a driver for switch from planktonic to biofilm lifestyle
ComplementarityDiversification of resource requirements leading to less competition between interspecific than conspecific neighborsMechanisms of coexistence under various light qualitiesB, G, Y, R, R:FR
Resource-based interactions
Resource competition Heterotrophic utilization of leaf lysates/organic compounds and their impact on secondary metabolites in microbial aggregate communitiesB, G, Y, R, R:FR
Phenotypic plasticityFormation of different phenotypes under various conditionsComplementary microbe pair for stimulating plant growth and pathogen controlB, R:FR
1 B = blue, 2 G = green, 3 Y = yellow; 4 R = red; 5 R:FR = red:far red.

© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (
Horticulturae EISSN 2311-7524 Published by MDPI AG, Basel, Switzerland RSS E-Mail Table of Contents Alert
Back to Top