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Protective and defensive roles of non-glandular trichomes against multiple stresses: structure–function coordination

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As superficial structures, non-glandular trichomes, protect plant organs against multiple biotic and abiotic stresses. The protective and defensive roles of these epidermal appendages are crucial to developing organs and can be attributed to the excellent combination of suitable structural traits and chemical reinforcement in the form of phenolic compounds, primarily flavonoids. Both the formation of trichomes and the accumulation of phenolics are interrelated at the molecular level. During the early stages of development, non-glandular trichomes show strong morphological similarities to glandular ones such as the balloon-like apical cells with numerous phenolics. At later developmental stages, and during secondary wall thickening, phenolics are transferred to the cell walls of the trichomes. Due to the diffuse deposition of phenolics in the cell walls, trichomes provide protection against UV-B radiation by behaving as optical filters, screening out wavelengths that could damage sensitive tissues. Protection from strong visible radiation is also afforded by increased surface light reflectance. Moreover, the mixtures of trichome phenolics represent a superficial chemical barrier that provides protection against biotic stress factors such as herbivores and pathogens. Although the cells of some trichomes die at maturity, they can modulate their quantitative and qualitative characteristics during development, depending on the prevailing conditions of the external biotic or abiotic environment. In fact, the structure and chemical constituents of trichomes may change due to the particular light regime, herbivore damage, wounding, water stress, salinity and the presence of heavy metals. Hence, trichomes represent dynamic protective structures that may greatly affect the outcome of many plant–environment interactions.


Superficial tissues (epidermis) and structures (cuticle and epidermal appendages) of plant organs play a crucial protecting role against multiple biotic and abiotic stress factors. As they comprise the outermost boundary between the plant and the environment, they mediate in a plethora of plant–environment interactions. Apart from their protective role against abiotic stress factors such as water losses, high UV and visible radiation intensities and temperature extremes, superficial tissues represent a barrier that has to be breached before any successful pathogen or herbivore attack can be established, and hence constitute the first line of plant defence. The protective (against abiotic stresses) and defensive (against biotic stresses) roles of these tissues and structures can be attributed to an excellent combination of suitable structural traits and chemical reinforcement in the form of secondary metabolites (LoPresti 2015). Among these compounds, phenolics play pivotal roles in chemical protection and defence located in the cuticle, the epidermis and (if present), in trichomes, either glandular or non-glandular. Given that the location of a given defensive/protective compound determines its ecological function (LoPresti 2015), and the selection of the optimal superficial protective-defensive mechanism is probably related to the successful survival in a particular environment (Agrawal et al. 2009), differences in leaf superficial structure and chemical composition are expected both at the inter- and intraspecific level, as well as along the various developmental stages. The variation in superficial structures of young leaves of different cultivars of grapevine (Vitis vinifera L.) is a good example of this selection at the intraspecific level. The surfaces of young leaves of different cultivars of grapevine may be glabrous-green (‘Soultanina’, syn. ‘Thompson Seedless’), or transiently have anthocyanins (e.g., ‘Siriki’) or pubescence (e.g., ‘Athiri’). Leaves possessing anthocyanins or trichomes are better protected against photoinhibition compared to the glabrous leaves. Photoinhibition is defined as the inhibition of photosynthesis due to damages in the photosynthetic machinery caused by the absorption of more photon energy than what can be used in the biochemical reactions and the risk of this phenomenon is higher in sunny environments (Demmig-Adams and Adams 2018). Both anthocyanins and trichome layers behave as optical filters, decreasing the intensity of the incident radiation received by the photosynthetic cells and thus decreasing the photoinhibition risk and consequently the xanthophyll cycle utilization rates (Morales et al 2002; Liakopoulos et al. 2006a; Galmés et al. 2007). In particular, the occurrence of non-glandular trichomes on leaf surfaces provides adaptive advantages under stressful environments by combining physical, mechanical and biochemical protection, especially in developing organs. To this respect, the current review focuses on the protective and defensive roles of non-glandular trichomes against multiple stresses, highlighting the coordination between trichome structural traits and phenolic deposition as a key component of the plant protective-defensive mechanism.

Non-glandular trichomes are protective epidermal appendages

Trichomes (or hairs) are defined as “unicellular or multi-cellular appendages, which originate from epidermal cells only, and develop outwards on the surface of various plant organs” (Werker 2000). The term “indumentum” describes the trichome layer of an organ as a whole. Investigation either of the individual structures or of the collective properties of the trichome layers (indumenta) began early in the XVII century (Johnson 1975). The ecophysiological roles of trichomes have been reviewed by Uphof (1962), Johnson (1975), Fahn (1986) and recently by Bickford (2016). The functions of trichomes and their bioinspired applications have also been recently reviewed by Liu et al. (2017a).

Trichomes can develop on the surface of all plant organs and are characterized as "glandular" or "non-glandular". The cells comprising the glandular trichomes can synthesize and secrete large quantities of compounds of the secondary metabolism, usually mixtures of terpenoids (as the main constituents) and phenolics (Werker 2000; Wagner et al. 2004; Huchelmann et al 2017; Lange and Srividya 2019). Non-glandular trichomes (the subject of the present review), do not possess a secretory mechanism and there are no analytical studies referring to the occurrence of high concentrations of terpenoids in these structures. However, non-glandular trichomes accumulate large quantities of phenolics, mainly at the early stages of their ontogeny (see next section), without apparent secretion ability. During these stages, however, young trichomes of olive (Olea europaea L.) and holm oak (Quercus ilex L.) leaves show high anatomical similarities to the glandular trichomes, such as the balloon-like apical cells characterised by thin cell walls (Galati 1982; Karabourniotis et al. 1998; Fig. 1).

Fig. 1

a Cross section of a young expanding leaf (second node) of Olea europaea under the fluorescence microscope. Excitation light is UV (exciter filter 330–385 nm/barrier filter 420 nm) and autofluorescence emitted is red–orange (chlorophyll of mesophyll tissues) or orange-yellow and yellow-green (phenolics, mainly flavonoids, from the cell walls of developed hairs (green arrows) and from the protoplast of young undeveloped hairs (white arrows). Black arrows show adaxial epidermis (ad) or abaxial epidermis (ab). Black bar shows mesophyll area. b Detail of the trichome layers of the adaxial leaf surface showing a developed hair and two undeveloped hairs on each side of the former. The one on the left is younger than the one on the right. In both undeveloped hairs, fluorescence is emitted by the protoplasm (yellow-green) and by the nuclei (yellow or green), the latter being due to perinuclear flavonoids. Scale bars: 200 μm. Microphotographs were taken with an Olympus BX40 fluorescent microscope equipped with an Olympus DP71 digital camera (Olympus Corporation, Japan)

Non-glandular trichomes are distinguished by their morphological characteristics and display a tremendous variability in their properties such as morphology, size and density often related to their functional purposes. For example, the presence of dense trichome layers is often considered a xeromorphic character (Fahn 1986; Karabourniotis et al. 1995; Körner 2003; Valkama et al. 2004; Moreno et al. 2010; Mershon et al. 2015; Amada et al. 2017). According to recent unpublished data of our research group deriving from a study on a typical Mediterranean ecosystem (Acarnanic Mountains in West Greece), we recorded that 57.7% of species of dwarf shrubs and perennial herbs in the study area had leaves with trichomes, while 26.2% were species with dense trichome layers. These life forms must tolerate the stressful conditions of the Mediterranean summer, i.e., the combination of high temperatures and light intensities and drought. However, it seems that this character is not limited to species of xerothermic sites and specific functional groups, given that a large amount of available data (Table 1) show that a significant part of the tree species of tropical rain forests (7.3–30%) have also densely pubescent leaves. The occurrence of dense trichome layers even in tropical species has also been related to protection against drought and high light intensity conditions (Ichie et al. 2016). However, data from different sites, life forms and functional groups are missing, highlighting the need for further studies that could offer valuable information on the function and evolutionary history of trichomes.

Table 1 Plant species with leaves bearing leaf trichomes (% of the species examined) thriving in different ecosystems of the world

Non-glandular trichomes contain phenolics associated with cell walls

The term “phenolic” is used to define carbon-based molecules that possess one (simple phenols) or more (polyphenols) phenolic groups (phenyl-groups), i.e. at least one hydroxyl-group bonded onto a benzyl ring (Quideau et al 2011). Phenolics are multifunctional secondary metabolites playing a wide array of defensive, protective and regulatory roles against either biotic or abiotic stress factors (Karabourniotis et al. 2014; Table 2). The phenolic content of non-glandular trichomes was analysed in a number of tree and shrub species with olive representing one of the most studied. Leaf trichomes of this species contain extractable phenolics, particularly flavonoids, non-covalently bound to the cell walls. The deposition of these compounds in the cell walls takes place during the short period of final trichome development, which corresponds to secondary wall thickening (Karabourniotis et al. 1998). Their composition differs from that of the internal pool, i.e., mesophyll and epidermal cell phenolics (Liakopoulos et al. 2006b). Although, quercetin 3-O-rutinoside and apigenin 7-O-glucoside located in leaf trichomes were also present in the lamina, quercetin, quercetin 3-O-rhamnoside and an unidentified flavone were located exclusively in the trichome layers (Liakopoulos et al. 2006b). The phenolics of mature trichomes are usually only a minor fraction of the total leaf pool (Liakopoulos et al. 2006b). Recently, molecular studies confirmed that mature olive trichomes are transcriptionally active, coding mainly for enzymes catalysing reactions involved in the biosynthesis of phenolics playing important protective and defensive roles (Koudounas et al. 2015). Roka et al. (2018) identified 249 proteins from olive mature trichomes which were classified to diverse groups such as “phosphorylation”, “response to stress” and “carbohydrate metabolic process” indicating that the cells of these structures are physiologically and biochemically active.

Table 2 Summary of the roles and actions of phenolics in plants

Flavonoids and other related compounds were also detected in non-glandular trichomes of leaves and fruits of other tree species. The leaf trichome layers of holm oak contain flavonoids and the main compounds are acylated kaempferol glycosides (Skaltsa et al 1994). Also, the trichomes covering the surface of peach cv. ‛Calrico’ are filled by polysaccharide material (63%) containing hydroxycinnamic acid derivatives (p-coumaric acid and ferulic acid) and flavonoids (Fernández et al. 2011). In some cases, the leaf surfaces are covered by anthocyanic-pigmented trichomes. The trichomes of young, developing leaves of the plane tree (Platanus orientalis L.) contain peonidin (Ntefidou and Manetas 1996) and the cauline trichomes of Plectranthus ciliatus contain peonidin 3,5-diglucosides with aromatic acylation with p-coumaric and sometimes caffeic acids (Jordheim et al. 2016). Anthocyanic trichomes are also present on the leaf surface of Castanopsis fissa (Zhang et al. 2016). The occurrence of phenolic compounds in trichome layers has also been reported for some characteristic shrubs of the Mediterranean ecosystem. In Cistus salvifolius L. leaves, the stalk cells and channel of the arm of non-glandular trichomes contain ellagitannins (punicalagin and two galloyl derivatives of punicalagin), whereas the trichome arms contain acylated kaempferol 3-O-glycosides associated with the cell wall (Tattini et al. 2007). El-Negoumy et al. (1986) reported that the leaf trichomes of Phlomis aurea and Phlomis floccosa contain 7-glucosides of naringenin, apigenin, luteolin and chrysoeriol and their acylated derivatives.

The occurrence of phenolic compounds in the trichome layers has been confirmed not only by analytical procedures but also by microscopic observations. Flavonoids (as well as other related phenolic compounds), show a bright yellow-green fluorescence following irradiation by blue light (Goodwin 1952; Rost 1995). Thus a number of histological studies confirmed the occurrence of these compounds in trichomes by epifluorescence microscopy (Karabourniotis and Fasseas 1996; Karabourniotis et al. 1998; Tattini et al. 2007; Stavrianakou et al. 2010; Karioti et al. 2011; Fernández et al. 2014; Koudounas et al. 2015; Fig. 1), and confocal laser scanning microscopy (Hützler et al. 1998; Fernadez et al. 1999). The occurrence of phenolic compounds in the trichome layers has also been confirmed histochemically (Tozin et al. 2016). Phenolics are not only detected in the soluble fraction of trichomes, but are also located in the cuticle (wax-bound) and in the cell wall insoluble fraction (esterified) of these structures (Liakopoulos et al 2006b; Fernández et al 2011; Mateu et al. 2016; Karabourniotis and Liakopoulos 2005). Moreover, flavonoids were also detected in the perinuclear region of the cells of young developing trichomes, indicating the need of special protection of this UV-sensitive organelle (Karabourniotis et al. 1998; Agati et al. 2012; Fig. 1).

The formation of trichomes and the accumulation of phenolics are interrelated at the molecular level

At the molecular level, the AtTTG1 (Arabidopsis thaliana (A. thaliana) TRANSPARENT TESTA GLABRA 1), the head of an evolutionarily conserved gene regulatory network, regulates both trichome formation and flavonoid (and anthocyanin) production throughout development (Xiao et al. 2017; Zhang and Schrader 2017). However, TTG1 was not identified in the trichomes of olive leaves (Koudounas et al. 2015). In Brassica rapa, the lipid transfer protein 2 (BraLTP2), which is expressed in leaf epidermal cells and trichomes, may play a role in both trichome development and accumulation of secondary metabolites, especially flavonoids (Tian et al. 2018). It seems, therefore, that both the formation of trichomes and the accumulation of phenolics are interrelated at the molecular level.

Coordinated structure (trichomes)-function (phenolics deposition) relationships and protection of plants against stresses

The multifunctionality of phenolic compounds indicates that resource allocation to these compounds in superficial tissues and especially in trichomes may render both defence against herbivores and pathogens, and protection against abiotic stresses. For example, flavonoids show a broad spectrum of functions for plants, including UV and high visible radiation protection, radical scavenging, pollination and feeding attraction, rhizosphere signalling and pathogen and herbivore defence (Iwashina 2003; Carletti et al. 2014; Mierziak et al. 2014; Agati and Tattini 2010; Siipola et al. 2015).

Protection from radiation

An important role of the trichome layer covering the surface of plant organs is the absorption of harmful UV-B radiation (Karabourniotis et al. 1992; Skaltsa et al. 1994; Ntefidou and Manetas 1996; Agati et al. 2012). The sensitivity to UV-B radiation is negatively correlated with the density of the trichomes, suggesting a UV-protective role for these structures (Liakoura et al. 1997; Yan et al. 2012). Indeed, trichomes act as shields against harmful wavelengths, offering protection to tissues against UV-B radiation (Karabourniotis et al. 1993, 1995; Grammatikopoulos et al. 1994; Skaltsa et al. 1994; Ripley et al. 1999; Manetas 2003; Tattini et al. 2007). This property of the trichome is attributed to the already mentioned diffuse deposition of phenolics in the cell walls (Strack et al. 1988; Karabourniotis et al. 1992, 1998; Skaltsa et al. 1994; Karabourniotis and Fasseas 1996; Ntefidou and Manetas 1996; Agati et al. 2012). Studies on olive and holm oak confirmed the optical role of trichomes by monitoring the light microenvironment beneath leaf trichome layers with fibre-optic microprobes. The trichome layers of the leaves in these two species attenuated almost all incident UV-B (310 nm) and UV-A (360 nm) radiation and a considerable portion of blue light (430 nm) (Karabourniotis and Bornman 1999; Karabourniotis et al. 1999). These light filtering and reflecting properties of the trichome layer may also render protection against visible radiation damage, especially in young leaves (Lang and Schindler 1994; Bisba et al. 1997; Karabourniotis and Bornman 1999; Karabourniotis et al. 1999; Zhang et al. 2016).

Plant–microorganism and plant–herbivore interactions

It is well known that trichomes represent permanent structures that offer physical protection against biotic stress factors. Concerning enemies, trichomes (including the glandular ones), influence insect oviposition and/or feeding in a wide range of insects and other herbivores (Levin 1973; Vermeij 2015). The occurrence of trichomes contributes to increased plant resistance against herbivores across different species of plants and affects tritrophic interactions (Riddick and Simmons 2014; Krimmel 2014). Moreover, trichomes are often composed of cellulose and other substances (such as phenolics) that are of low nutritional value for the insects (Levin 1973).

Concerning pathogens, trichomes act as a passive screen that prevent spores and other microbial structures from reaching the leaf surface or forming a water repellent surface preventing the formation of water films on which pathogens might be deposited and germinate or multiply (Johnson 1975; Allen et al. 1991; Mmbaga and Staedman 1992; Mmbaga et al. 1994; Kortekamp and Zyprian 1999; Kortekamp et al. 1999; Bradley et al. 2003; Agrios 2005; Fernández et al. 2014).

However, not only the physical but also the chemical characteristics of the superficial tissues and structures affect the success or failure of microbial growth on, and subsequently, within the leaf (Allen et al. 1991). Microbial growth on leaf surfaces is usually favoured when rain or dew creates an aqueous film on the lamina (Romantschuk et al. 1996). The inducible plant defence mechanisms do not reach the external surface of an unwounded organ, but the presence of aqueous films on leaf surfaces may cause leaching of substances present in superficial tissues and structures (Reigosa et al. 1999). These leachates may include substances that restrict or prevent the growth of phytopathogens such as terpenoids and phenolic compounds (Inderjit et al. 1999; Reigosa et al. 1999; Mithöfer and Maffei 2016). Flavonoids and other polyphenol constituents may be toxic to bacteria, fungi and insects and/or have allelopathic properties (Pourcel et al. 2006; Weston and Mathesius 2013). Thus the occurrence of mixtures of phenolics in trichomes may provide a preformed chemical line of defence of plant surfaces against biotic stress factors. The antimicrobial activity of these compounds may be enhanced by the synergistic action of UV-A radiation (Shirai and Yasumoto 2019). Given that these substances are non-covalently bound to the cell walls of the trichomes), they can be leached out by water (Fig. 2) and create a chemically adverse environment against the entrance and spreading of pathogens in the leaf interior. Indeed, aqueous extracts from isolated non-glandular leaf trichomes of olive and holm oak at realistic concentrations (resembling those of the leaf surface), inhibit the growth of the majority of the phytopathogenic bacteria as well as the spore germination and growth of various fungi species (Stavrianakou et al. 2010). This defensive ability seems to be age-dependent because the leached substances are not replaced (the trichomes of olive and holm oak are dead at maturity, see Fahn 1986; Karabourniotis et al. 1998). Therefore, trichomes of older leaves contain lower concentrations of polyphenol compounds per unit dry mass than younger, fully expanded leaves, probably due to leaching during the growth period (Karabourniotis et al. 1998). In a recent study, Rennberger et al. (2017) showed that trichome density and length, as well as polyphenol autofluorescence of epidermis and trichomes were negatively correlated with the susceptibility of members of the Cucurbitaceae family to Didymella bryoniae, the causal agent of gummy stem blight.

Fig. 2

HPLC profiles of methanolic (ME) and aqueous (AE) extracts of non-glandular leaf hairs of Olea europaea, as well as of aqueous leachates (AL) of leaves after a leaching time of 4 h. Insert graph shows the relative abundance of phenolic compounds in extracts (ME, AE) and aqueous leachates (AL) by means of absorbance at 300 nm

Other functions not related to the occurrence of phenolic compounds in trichomes

A number of additional protective roles have been ascribed to trichomes, not directly related to the deposition of phenolic compounds in these structures. Dense trichome layers may prevent water losses, either directly by influencing the thickness of the boundary layer and hence the respective resistance to water vapour diffusion from the transpiring leaf surface, or indirectly by regulating the energy balance and thus the temperature of the lamina (Nobel 1983; Ehleringer 1984; Fahn and Cutler 1992; Schuepp 1993; Holmes and Keiller 2002; Pshenichnikova et al. 2019). Trichomes also affect the water–leaf surface interactions (leaf wettability, droplet retention or repellence), and contribute to plant water uptake and water balance (Savé et al. 2000; Fernández et al. 2014; Konrad et al. 2014; Bickford 2016; Hu et al. 2019).

There is also evidence that leaf trichomes of a number of plants, including A. thaliana, take part in the detoxification of heavy metals (Blamey et al. 1986; Ager et al. 2003; Broadhurst et al. 2004; Domínguez-Solís et al. 2004). There are, however, reports that in certain hyperaccumulators, heavy metals are consistently concentrated at the base of leaf trichomes or epidermal cells but are excluded from trichomes (Krämer et al. 1997; Küpper et al. 2000; Psaras et al. 2000; Zhao et al. 2000). These contradictory reports could be attributed to the physiological differences between species, since some trichomes are dead at maturity (as mentioned previously), and thus unable to accumulate metals. The accumulation of toxic molecules within trichomes may decrease the nutritional value of the plant and therefore deter herbivore feeding. This function may be related to the presence of phenolics in trichome cells, as these compounds show metal chelating activity (Michalak 2006).

Leaf epidermal appendances such as glandular or non-glandular trichomes may also interact with atmospheric pollutants such as ozone. High levels of tropospheric ozone negatively affect the growth, the development as well as the productivity of plants, both in a short- and long-term basis. O3 is characterized as a toxic, strong polar oxidant which is diffused to the plant interior mainly through stomata. Leaf epidermal appendances increase the active leaf area and favor the maintenance of a thick and moist boundary layer which can act as an ozone sink (Wieser 2002). Moreover, leaf surface reactions can scavenge O3, acting as an additional sink for O3 before it enters the leaf. For example, semi-volatile organic compounds (such as the diterpenoid cis-abienol), secreted by the glandular trichomes of Nicotiana tabacum act as an efficient O3 sink (Jud et al. 2016). Thus glandular trichomes constitute a chemical barrier that reduces leaf ozone uptake and toxicity (Li et al. 2018; Oksanen 2018; Prozherina et al. 2003). This function is positively correlated with the density of glandular trichomes but not with non-glandular ones (Li et al 2018). In plants growing with high levels of Ca2+, trichomes play a key role in the regulation of the apoplastic concentration of this element. Ozone has a detrimental effect on the ability of trichomes to regulate the concentration of apoplastic Ca2+, resulting in altered stomatal behavior, possibly due to the disruption of guard-cell Ca2+-mediated signal transduction (De Silva et al. 2001).

Trichomes can also act as traps, accumulating atmospheric particles and dust and thus enhance the filtering capacity of the plant species (Sæbø et al. 2012; Ram et al. 2015; Muhammad et al. 2019). The indumentum represents an optimum zone of particle deposition because it increases the active leaf area and creates a rough surface (De Nicola et al. 2008). Pubescent leaves have been shown to exhibit greater entrapping ability than glabrous ones, both for inorganic and organic contaminants (Little and Wiffen 1977; Howsam et al. 2000; Hu et al. 2019). This capability gives rise to inspirations for efficient oil spill cleanup materials (Zeiger et al. 2016).

Recently, it was proposed that A. thaliana trichomes could act as sensors responding to mechanical and acoustic stimuli. Zhou et al. (2016) proposed that trichomes behave as an active mechanosensor, converting physical signals such as mechanical touch from insects into chemical signals like calcium oscillation and pH shift of skirt cells to elicit various defensive reactions. The mechanic stimuli could also be combined with vibrational stimulation of A. thaliana trichomes associated with feeding caterpillars (Liu et al. 2017b).

Trichomes: preformed but not static structures

As mentioned previously, the occurrence of a dense layer of non-glandular trichomes has been considered as a preformed mechanical barrier for non-specific plant resistance to pathogens and herbivorous insects, or a preformed layer for protection against intense radiation and water losses. The trichome layers of mature leaves, and possibly of other organs, are considered as a fixed and static protective characteristic because usually the trichome cells are dead at maturity, hence there is no chance for further structural or biochemical alterations. However, trichome layers can change their characteristics during development (for a recent review see Hauser 2014). For example, a mature olive leaf invests up to 10% of its dry mass in the trichome layers, whereas young leaves invest more than 40% (Karabourniotis et al. 1995). Moreover, during these stages, the developing non-glandular trichomes resemble the glandular ones morphologically and possibly functionally, due to the very high concentration of phenolics contained in their cells (Karabourniotis et al. 1995; Karabourniotis and Fasseas 1996; Fig. 1). In the young leaves of olive trees, a high portion (up to 70%) of their phenolic pool is deposited in trichome layers (Karabourniotis et al. 1995). Therefore, the protective role of the trichome against biotic and abiotic factors is particularly significant during early stages of leaf development and may be less important at later stages, namely, when protection is taken over by the epidermis (Karabourniotis and Fasseas 1996; Valkama et al. 2004; Calixto et al. 2015). Furthermore, young leaves of many plant species are pubescent on both surfaces, but as they develop, the adaxial trichome is progressively lost and the protective role is undertaken by the epidermis (Karabourniotis et al. 1995). The occurrence of trichome layers on the abaxial surface of mature leaves is possibly related to the protection of stomata against water losses and intense radiation (Karabourniotis et al. 1993; Grammatikopoulos et al. 1994).

Leaves can also modify trichome quantitative and qualitative characteristics according to the conditions that prevail in the external biotic or abiotic environment. The structure and chemical constituents of trichomes may change upon herbivore damage or artificial wounding (Larkin et al. 1996; Yoshida et al. 2009). The response of some plants to herbivore damage includes the development of new leaves with an increased density and/or number of trichomes (Traw and Bergelson 2003). This inducible defence response in A. thaliana is controlled by jasmonic and salicylic acid (Traw and Bergelson 2003). Insects feeding on these new acclimated leaves often consume less biomass and show limited growth compared to insects feeding on non-acclimated leaves (Baur et al. 1991; Dalin et al. 2008). In some cases, the feeding of eriophyoid mites on leaf surfaces can cause erinea formation, e.g., a hyperplasia of the leaf trichomes (Karioti et al. 2011). In holm oak leaves, the hypertrophic trichomes accumulate pigments responsible for the red-brown coloration of the erineum. The cells of these trichomes have thinner walls and contain higher concentrations of proanthocyanidin B3, catechin and quercetin-3-O-glucoside, but lower concentrations of acylated flavonoid glycosides than normal ones (Karioti et al. 2011). Taking into account that the first two compounds are referred to as feeding deterrents, these changes in trichome anatomy and chemistry may restrict the damage caused by the mites (Karioti et al. 2011).

The structure and chemical constituents of trichomes may also change according to the light regime during leaf development. Exposure of developing leaves to high light intensities induces qualitative and quantitative changes in the phenolic content of trichomes, with the possible formation of new flavonoid compounds (Ntefidou and Manetas 1996; Liakoura et al. 1997). The UV-absorbing capacity and the density of the trichomes of leaves exposed to UV-B radiation were higher compared to those of shaded leaves (Liakoura et al. 1997; Václaník et al. 2017). In several A. thaliana trichome mutants and wild-type plants, the exposure to UV-B radiation caused a significant increase in trichome density, suggesting that trichome formation was induced by UV-B (Yan et al. 2012). qRT-PCR analysis indicated that the control of trichome initiation by UV-B radiation is integrated through the expression of a GLABRA3 (GL3) transcription factor (Yan et al. 2012; Kulich et al. 2015). GL3 is a key transcription factor not only of UV-induced, but also of wound-induced trichome formation in A. thaliana. In the last case, GL3 acts downstream of jasmonic acid signalling (Yoshida et al. 2009; Hauser 2014). Continuous UV-B irradiation causes an increase in the number of cells and in the polyphenolic content of the trichomes (Yamasaki et al. 2007; Yamasaki and Murakami 2014). Trichome formation was also increased in plants grown under water stress, such as barley (Liu and Liu 2016), aubergine (Fu et al. 2013), olive (Boughalleb and Hajlaoui 2011), eggplant (Fu et al. 2013) and tomato (Galdon-Armero et al. 2018). Similar results were also observed under saline conditions (Çelik et al. 2018). In contrast, trichome density was reduced in leaves of Pb-treated plants (Koul and Bhatnagar 2017).


Plant trichomes constitute a superficial, protective and quite dynamic tissue that, during its development, is able to respond to an abundance of cues. During both their early life and after development, they exhibit a plethoric character, distinct optical and mechanical properties and a very rich, leachable and complex mixture of secondary metabolites. Therefore, trichomes prevail on plant surfaces exposed to the surrounding environment and determine the outcome of many abiotic and biotic interactions. Trichomes represent an important plant trait that should always be accounted in the perpetual pursuit for more stress tolerance characters in plants.


  1. Agati G, Tattini M (2010) Multiple functional roles of flavonoids in photoprotection. New Phytol 186(4):786–793

  2. Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci 196:67–76

  3. Ager FJ, Ynsa JR, Dominguez-Solis Lopez-Martin MC, Gotor C, Romero LC (2003) Nuclear micro-probe analysis of Arabidopsis thaliana leaves. Nucl Instrum Methods Phys Res Sect B Beam Interact Mater At 210:401–406

  4. Agrawal AA, Fishbein M, Jetter R, Salminen JP, Goldstein JB, Freitag AE, Sparks JP (2009) Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol 183:848–867

  5. Agrios G (2005) Plant pathology, 5th edn. Academic Press, London, p 952

  6. Allen EA, Hoch HC, Steadman JR, Stavely RG (1991) Influence of leaf surface on spore deposition and the epiphytic growth of phytopathogenic fungi. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 87–110

  7. Amada G, Onoda Y, Ichie T, Kitayama K (2017) Influence of leaf trichomes on boundary layer conductance and gas-exchange characteristics in Metrosideros polymorpha (Myrtaceae). Biotropica 49:482–492

  8. Baur R, Binder S, Benz G (1991) Non glandular leaf trichomes as short-term inducible defence of the grey alder, Alnus incana (L.), against the chrysomelid beetle Agelastica alni L. Oecologia 87:219–226

  9. Bickford CP (2016) Ecophysiology of leaf trichomes. Funct Plant Biol 43(9):807–814

  10. Bisba A, Petropoulou Y, Manetas Y (1997) The transiently pubescent young leaves of plane (Platanus orientalis) are deficient in photodissipative capacity. Physiol Plant 101:373–378

  11. Blamey FPC, Joyce DC, Edwards DG, Asher CJ (1986) Role of trichomes in sunflower tolerance to manganese toxicity. Plant Soil 91:171–180

  12. Boeger MRT, Alves LC, Negrelle RRB (2004) Leaf morphology of 89 tree species from a lowland tropical rain forest (Atlantic forest) in South Brazil. Braz Arch Biol Technol 47:933–943

  13. Bongers F, Popma J (1990) Leaf characteristics of the tropical rain forest flora of Los Tuxtlas, Mexico. Bot Gaz 151:354–365

  14. Boughalleb F, Hajlaoui H (2011) Physiological and anatomical changes induced by drought in two olive cultivars (cv. Zalmati and Chemlali). Acta Physiol Plant 33:53–65

  15. Bradley DJ, Gilbert GS, Parker IM (2003) Susceptibility of clover species to fungal infection: the interaction of leaf surface traits and environment. Am J Bot 90:857–864

  16. Broadhurst CL, Chaney RL, Angle JS, Maugel TK, Erbe EF, Murphy CA (2004) Simultaneous hyperaccumulation of nickel, manganese, and calcium in Alyssum leaf trichomes. Environ Sci Technol 38:5797–5802

  17. Calixto ES, Lange D, Del-Claro K (2015) Foliar anti-herbivore defences in Qualea multiflora Mart. (Vochysiaceae): changing strategy according to leaf development. Flora 212:19–23

  18. Carletti G, Nervo G, Cattivelli L (2014) Flavonoids and melanins: a common strategy across two kingdoms. Int J Biol Sci 10:1159–1170

  19. Çelik Ö, Atak Ç, Suludere Z (2018) Comparative transcriptional profiling of soybean orthologs of Arabidopsis trichome developmental genes under salt stress. Plant Mol Biol Report 36:82–93

  20. Dalin P, Ågren J, Bjorkman C, Huttunen P, Kärkkäinen K (2008) Leaf trichome formation and plant resistance to herbivory. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Berlin, pp 89–105

  21. De Nicola F, Maisto G, Prati MV, Alfani A (2008) Leaf accumulation of trace elements and polycyclic hydrocarbons (PAHs) in Quercus ilex L. Environ Pollut 153:376–383

  22. De Silva LD, Mansfield TA, McAinsh MR (2001) Changes in stomatal behaviour in the calcicole Leontodon hispidus due to the disruption by ozone of the regulation of apoplastic Ca2+ by trichomes. Planta 214:158–162

  23. Demmig-Adams B, Adams WW (2018) An integrative approach to photoinhibition and photoprotection of photosynthesis. Environ Exp Bot 154:1–3

  24. Domínguez-Solís JR, López-Martín MC, Ager FJ, Ynsa MD, Romero LC, Gotor C (2004) Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotech J 2(6):469–476

  25. Ehleringer JR (1984) Ecology and ecophysiology of leaf pubescence in North America desert plants. In: Healy PL, Mehta I, Rodriguez E(eds) Biology and chemistry of plant trichomes. Plenum Publishing Corporation, New York, pp 113–132

  26. El-Negoumy SI, Abdalla MF, Saleh NAM (1986) Flavonoids of Phlomis aurea and P. floccosa. Phytochemistry 25:772–774

  27. Fahn A (1986) Structural and functional properties of trichomes of xeromorphic leaves. Ann Bot 57:631–637

  28. Fahn A, Cutler D (1992) Xerophytes. Gebruder Borntraeger, Berlin, p 176

  29. Fernadez S, Osorio S, Heredia A (1999) Monitoring and visualising plant cuticles by confocal laser scanning microscopy. Plant Physiol Biochem 37:789–794

  30. Fernández V, Khayet M, Montero-Prado P, Heredia-Guerrero J, Liakopoulos G, Karabourniotis G, del Río V, Domínguez E, Tacchini I, Nerín C, Val J, Heredia A (2011) New insights into the properties of pubescent surfaces: peach fruit as a model. Plant Phys 156:2098–2108

  31. Fernández V, Sancho-Knapik D, Guzmán P, Peguero-Pina JJ, Gil L, Karabourniotis G, Khayet M, Fasseas C, Heredia-Guerrero JA, Heredia A, Gil-Pelegrín E (2014) Wettability, polarity, and water absorption of holm oak leaves: effect of leaf side and age. Plant Phys 166:168–180

  32. Fu QS, Yang RC, Wang HS, Zhao B, Zhou CL, Ren SX, Guo Y-D (2013) Leaf morphological and ultrastructural performance of eggplant (Solanum melongena L.) in response to water stress. Photosynthetica 51(1):109–114

  33. Galati BG (1982) Ontogenia de los trichomes de Olea europaea L. (Oleaceae). Physis (B. Aires) 41:65–71

  34. Galdon-Armero J, Fullana-Pericas M, Mulet PA, Conesa MA, Martin C, Galmes J (2018) The ratio of trichomes to stomata is associated with water use efficiency in Solanum lycopersicum (tomato). Plant J 96:607–619

  35. Galmés J, Medrano H, Flexas J (2007) Photosynthesis and photoinhibition in response to drought in a pubescent (var. minor) and a glabrous (var. palaui) variety of Digitalis minor. Environ Exp Bot 60:105–111

  36. Goodwin RH (1952) Fluorescence substances in plants. Bot Rev 3:283–304

  37. Grace SC (2007) Phenolics as antioxidants. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell, Hoboken, pp 141–196

  38. Grammatiκopoulos G, Karabourniotis G, Kyparissis A, Petropoulou Y, Manetas Y (1994) Leaf hairs of olive (Olea europaea L.) prevent stomatal closure by ultraviolet-B radiation. Aust J Plant Physiol 21:293–301

  39. Grubb PJ, Grubb EAA, Miyata I (1975) Leaf structure and function in evergreen trees and shrubs of Japanese warm temperate rain forest. I. The structure of the lamina. Bog Mag Tokyo 88:197–211

  40. Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243

  41. Hauser M-T (2014) Molecular basis of natural variation and environmental control of trichome patterning. Front Plant Sci 5:320

  42. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

  43. Holmes M, Keiller D (2002) Effects of pubescence and waxes on the reflectance of leaves in the ultraviolet and photosynthetic wavebands: a comparison of a range of species. Plant Cell Environ 25:85–93

  44. Howsam M, Jones KC, Ineson P (2000) PAHs associated with leaves of three deciduous tree species. I - Concentrations and profiles. Environ Pollut 108:413–424

  45. Hu YB, Peuke AD, Zhao XY, Yan JX, Li CM (2019) Effects of simulated atmospheric nitrogen deposition on foliar chemistry and physiology of hybrid poplar seedlings. Plant Physiol Biochem 143:94–108

  46. Huchelmann A, Boutry M, Hachez C (2017) Plant glandular trichomes: natural cell factories of high biotechnological interest. Plant Phys 175(1):6–22

  47. Hützler P, Fieschbach R, Heller W, Jungblut TP, Reuber S, Schmitz M, Veit M, Weissenboeck G, Schnitzler J-P (1998) Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. J Exp Bot 49:953–965

  48. Ichie T, Inoue Y, Takahashi N, Kamiya K, Kenzo T (2016) Ecological distribution of leaf stomata and trichomes among tree species in a Malaysian lowland tropical rain forest. J Plant Res 129:625–635

  49. Inderjit K, Cheng HH, Nishimura H. 1999. Plant Phenolics and terpenoids: transformation, degradation and potential for allelopathic interactions. In: Inderjit K, Dakshini MM, Foy CL (eds) Principles and practices in plant ecology. CRC Press, Boca Raton, pp 255–266

  50. Iwashina T (2003) Flavonoid function and activity to plants and other organisms. Biol Sci Space 17:24–44

  51. Jansen MA, Coffey AM, Prinsen E (2012) UV-B induced morphogenesis: four players or a quartet? Plant Signal Behav 7:1185–1187

  52. Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev 41:233–258

  53. Jordheim M, Calcott K, Gould KS, Davies KM, Schwinn KE, Andersen ØM (2016) High concentrations of aromatic acylated anthocyanins found in cauline hairs in Plectranthus ciliates. Phytochemistry 128:27–34

  54. Jud W, Fischer L, Canaval E, Wohlfahrt G, Tissier A, Hansel A (2016) Plant surface reactions: an ozone defence mechanism impacting atmospheric chemistry. Atmos Chem Phys 16:277–292

  55. Karabourniotis G, Bornman JF (1999) Penetration of UV-A, UV-B and blue light through the leaf trichome layers of two xeromorphic plants, olive and oak, measured by optical fibre microprobes. Phys Plant 105:655–661

  56. Karabourniotis G, Fasseas C (1996) The dense indumentum with its polyphenol content may replace the protective role of the epidermis in some young xeromorphic leaves. Can J Bot 74:347–351

  57. Karabourniotis G, Liakopoulos G (2005) Phenolic compounds in plant cuticles: physiological and ecological aspects. Adv Plant Phys 8:33–47

  58. Karabourniotis G, Papadopoulos K, Papamarkou M, Manetas Y (1992) Ultraviolet-B radiation absorbing capacity of leaf hairs. Phys Plant 86:414–418

  59. Karabourniotis G, Kyparissis A, Manetas Y (1993) Leaf hairs of Olea europaea L. protect underlying tissues against ultraviolet-B radiation damage. Environ Exp Bot 33:341–345

  60. Karabourniotis G, Kotsabassidis D, Manetas Y (1995) Trichome density and its protective potential against ultraviolet-B radiation damage during leaf development. Can J Bot 73:376–383

  61. Karabourniotis G, Kofidis G, Fasseas C, Liakoura V, Drossopoulos I (1998) Polyphenol deposition in leaf hairs of Olea europaea (Oleaceae) and Quercus ilex (Fagaceae). Am J Bot 85:1007–1012

  62. Karabourniotis G, Bornman JF, Liakoura V (1999) Different leaf surface characteristics of three grape cultivars affect leaf optical properties as measured with fibre optics. Possible implication in Stress tolerance. Aust J Plant Phys 26:47–53

  63. Karabourniotis G, Liakopoulos G, Nikolopoulos D, Bresta P, Stavroulaki V, Sumbele S (2014) Carbon gain vs. water saving, growth vs. defence: two dilemmas with soluble phenolics as a joker. Plant Sci 227:21–27

  64. Karioti A, Tooulakou G, Bilia AR, Psaras GK, Karabourniotis G, Skaltsa H (2011) Erinea formation on Quercus ilex leaves: anatomical, physiological and chemical responses of leaf hairs against mite attack. Phytochemistry 72:230–237

  65. Konrad W, Burkhardt J, Ebner M, Roth-Nebelsick A (2014) Leaf pubescence as a possibility to increase water use efficiency by promoting condensation. Ecohydrology 8:480–492

  66. Körner C (2003) Alpine plant life. Springer, Berlin, Berlin, p 338

  67. Kortekamp A, Zyprian E (1999) Leaf hairs as a basic protective barrier against downy mildew of grape. J Phytopathol 147:453–459

  68. Kortekamp A, Wind R, Zyprian E (1999) The role of hairs on the wettability of grapevine (Vitis spp.) leaves. Vitis 38:101–105

  69. Koudounas K, Manioudaki ME, Kourti A, Banilas G, Hatzopoulos P (2015) Transcriptional profiling unravels potential metabolic activities of the olive leaf non-glandular trichome. Front Plant Sci 6:633

  70. Koul M, Bhatnagar AK (2017) Changes in the leaf epidermal features of Cyamopsis tetragonoloba (L.) Taub. in response to lead in soil. Phytomorphology 67:1–1

  71. Krämer U, Grime GW, Smith JAC, Hawes CR, Baker AJM (1997) Micro-PIXE as a technique for studying nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum. Nucl Instrum Methods Phys Res B 130(1):346–350

  72. Krimmel BA (2014) Why plant trichomes might be better than we think for predatory insects. Pest Manag Sci 70(11):1666–1667

  73. Kulich I, Vojtíková Z, Glanc M, Ortmannová J, Rasmann S, Zárský V (2015) Cell wall maturation of Arabidopsis trichomes is dependent on exocyst subunit EXO70H4 and involves callose deposition. Plant Phys 168:120–131

  74. Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other metals in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84

  75. Lang M, Schindler C (1994) The effect of leaf-hairs on blue and red fluorescence emission and on zeaxanthin cycle performance of Senecio medley L. J Plant Phys 144:680–685

  76. Lange BM, Srividya N (2019) Enzymology of monoterpene functionalization in glandular trichomes. J Exp Bot 70:1095–1108

  77. Larkin JC, Young N, Prigge M, Marks MD (1996) The control of trichome spacing and number in Arabidopsis. Development 122:997–1005

  78. Levin DA (1973) The role of trichomes in plant defence. Q Rev Biol 48:3–14

  79. Li S, Tosens T, Harley PC, Harley PC, Jiang Y, Kanagendran A, Grosberg M, Jaamets K, Niinemets Ü (2018) Glandular trichomes as a barrier against atmospheric oxidative stress: relationships with ozone uptake, leaf damage, and emission of LOX products across a diverse set of species. Plant Cell Environ 41:1263–1277

  80. Liakopoulos G, Nikolopoulos D, Klouvatou A, Vekkos KA, Manetas Y, Karabourniotis G (2006a) The photoprotective role of epidermal anthocyanins and surface pubescence in young leaves of grapevine (Vitis vinifera). Ann Bot 98:257–265

  81. Liakopoulos G, Stavrianakou S, Karabourniotis G (2006b) Trichome layers versus dehaired lamina of Olea europaea leaves: differences in flavonoid distribution, UV-absorbing capacity, and wax yield. Environ Exp Bot 55:294–304

  82. Liakoura V, Stefanou M, Manetas Y, Cholevas C, Karabourniotis G (1997) Trichome density and iIts UV-B protective potential are affected by shading and leaf position on the canopy. Environ Exp Bot 38:223–229

  83. Little P, Wiffen RD (1977) Emissions and deposition of petrol engine exhaust Pb-I. Deposition of exhaust Pb to plant and soil surface. Atmos Environ 11:437–447

  84. Liu X, Liu C (2016) Effects of drought-stress on Fusarium crown rot development in barley. 688 PLOS ONE 11:e0167304

  85. Liu H, Liu S, Jiao J, Lubc TJ, Xu F (2017a) Trichomes as a natural biophysical barrier for plants and their bioinspired applications. Soft Matter 13:5096–5106

  86. Liu S, Jiao J, Lu TJ, Xu F, Pickard BG, Genin GM (2017b) Arabidopsis leaf trichomes as acoustic antennae. Biophys J 113:2068–2076

  87. LoPresti EF (2015) Chemicals on plant surfaces as a heretofore unrecognized, but ecologically informative, class for investigations into plant defence. Biol Rev 91:1102–1117

  88. Mandal D, Chakrabotry S, Dey S (2010) Phenolic acids act as signalling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368

  89. Manetas Y (2003) The importance of being hairy: the adverse effects of hair removal on stem photosynthesis of Verbascum speciosum are due to solar UV-B radiation. New Phytol 158:503–508

  90. Mateu BP, Hauser MT, Heredia A, Gierlinger N (2016) Waterproofing in Arabidopsis: following phenolics and lipids in situ by confocal raman microscopy. Front Chem 4:10

  91. Mershon JP, Becker M, Bickford CP (2015) Linkage between trichome morphology and leaf optical properties in New Zealand alpine Pachycladon (Brassicaceae). New Zeal J Bot 53:175–182

  92. Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish J Environ Stud 15(4):523–530

  93. Mierziak J, Kostyn K, Kulma A (2014) Flavonoids as important molecules of plant interactions with the environment. Molecules 19:16240–16265

  94. Mithöfer A, Maffei ME (2016) General mechanisms of plant defense and plant toxins. In: Gopalakrishnakone P, Carlini CR, Ligabue-Braun R (eds) Plant toxins. Springer, Berlin, pp 1–22

  95. Mmbaga MT, Steadman JR (1992) Adult-plant resistance associated with leaf pubescence in common bean. Plant Dis 76:1230–1236

  96. Mmbaga MT, Steadman JR, Roberts JJ (1994) Interaction of bean leaf pubescence with rust urediniospore deposition and subsequent infection density. Ann Appl Biol 125:243–254

  97. Morales F, Abadía A, Abadía J, Montserrat G, Gil-Pelegrín E (2002) Trichomes and photosynthetic pigment composition changes: responses of Quercus ilex subsp. ballota (Desf.) Samp. and Quercus coccifera L. to Mediterranean stress conditions. Trees 16:504–510

  98. Moreno L, Bertiller MB, Carrera AL (2010) Changes in traits of shrub canopies across an aridity gradient in northern Patagonia, Argentina. Basic Appl Ecol 11:693–701

  99. Muhammad S, Wuyts K, Samson R (2019) Atmospheric net particle accumulation on 96 plant species with contrasting morphological and anatomical leaf characteristics in a common garden experiment. Atmos Env 202:328–344

  100. Nobel PS (1983) Biophysical plant physiology and ecology. WH Freeman and Co, San Francisco

  101. Ntefidou M, Manetas Y (1996) Optical properties of hairs during the early stages of leaf development in Platanus orientalis. Aust J Plant Physiol 23:535–538

  102. Oksanen E (2018) Trichomes form an important first line of defence against adverse environment—new evidence for ozone stress mitigation. Plant Cell Environ 41:1497–1499

  103. Pourcel L, Routaboul J-M, Cheynier V, Lepiniec L, Debeaujon I (2006) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12:29–36

  104. Pringle EG, Adams RI, Broadbent E, Busby PE, Donatti CI, Kurten EL, Renton K, Dirzo R (2011) Distinct leaf-trait syndromes of evergreen and deciduous trees in a seasonally dry tropical forest. Biotropica 43:299–308

  105. Prozherina N, Freiwald V, Rousi M, Oksanen E (2003) Interactive effect of springtime frost and elevated ozone on early growth, foliar injuries and leaf structure of birch (Betula pendula). New Phytol 159:623–636

  106. Psaras GK, Constantinidis TH, Cotsopoulos B, Manetas Y (2000) Relative abundance of nickel in the leaf epidermis of eight hyperaccumulators: evidence that the metal is excluded from both guard cells and trichomes. Ann Bot 86:73–78

  107. Pshenichnikova TA, Doroshkov AV, Osipova SV, Permyakov AV, Permyakova MD, Efimov VM, Afonnikov DA (2019) Quantitative characteristics of pubescence in wheat (Triticum aestivum L.) are associated with photosynthetic parameters under conditions of normal and limited water supply. Planta 249:839–847

  108. Pyykkö M (1979) Morphology and anatomy of leaves from some woody plants in a humid tropical rainforest of Venezuelan Guayana. Acta Bot Fenn 112:1–41

  109. Quideau SP, Deffieux D, Douat-Casassus CL, Pouységu L (2011) Plant polyphenols: chemical properties, biological activities, and synthesis. Angew Chem Int Ed 50:586–621

  110. Ram SS, Majumder S, Chaudhuri P, Chanda S, Santra SC, Chakraborty A, Sudarshan M (2015) A review on air pollution monitoring and management using plants with special reference to foliar dust adsorption and physiological stress responses. Crit Rev Environ Sci Technol 45(23):2489–2522

  111. Reigosa MJ, Sánchez-Moreiras A, González L (1999) Ecophysiological approach in allelopathy. Crit Rev Plant Sci 18:577–608

  112. Rennberger G, Keinath AP, Hess M (2017) Correlation of trichome density and length and polyphenol fluorescence with susceptibility of five cucurbits to Didymella bryoniae. J Plant Dis Prot 124:313

  113. Riddick EW, Simmons AM (2014) Do plant trichomes cause more harm than good to predatory insects? Pest Manag Sci 70:1655–1665

  114. Ripley BS, Pammenter NW, Smith VR (1999) Function of leaf hairs revisited: the hair layer on leaves Arctotheca populifolia reduces photoinhibition, but leads to higher leaf temperatures caused by lower transpiration rates. J Plant Phys 155:78–85

  115. Roka L, Koudounas K, Daras G, Zoidakis J, Vlahou A, Kalaitzis P, Hatzopoulos P (2018) Proteome of olive non-glandular trichomes reveals protective protein network against (a)biotic challenge. J Plant Phys 231:210–218

  116. Romantschuk M, Roine E, Björklöf K, Ojanen T, Nurmiaho-Lassila E-L, Haahtela K (1996) Microbial attachment to plant aerial surfaces. In: Morris CG, Nicot PC, Nguyen C (eds) Aerial plant surface microbiology. Plenum Press, New York, pp 43–58

  117. Rost FWD (1995) Fluorescence microscopy, vol II. Cambridge University Press, New York

  118. Roth I (1984) Stratification of tropical forests as seen in leaf structure. Dr W Junk Publishers, Hague, p 246

  119. Sæbø A, Popek R, Nawrot B, Hanslin HM, Gawronska H, Gawronski SW (2012) Plant species differences in particulate matter accumulation on leaf surfaces. Sci Total Environ 427–428:347–354

  120. Savé R, Biel C, de Herralde F (2000) Leaf pubescence, water relations and chlorophyll fluorescence in two subspecies of Lotus Creticus L. Biol Plant 43:239–244

  121. Schreiner M, Mewis I, Huyskens-Keil S, Jansen MAK, Zrenner R, Winkler JB, O’Brien N, Krumbein A (2012) UV-B-induced secondary plant metabolites—potential benefits for plant and human health. Crit Rev Plant Sci 31(3):229–240

  122. Schuepp PH (1993) Leaf boundary layers. New Phytol 125:477–507

  123. Shirai A, Yasutomo Y-K (2019) Bactericidal action of ferulic acid with ultraviolet-A light irradiation. J Photochem Photobiol B Biol 191:52–58

  124. Siipola SM, Kotilainen T, Sipari N, Morales LO, Lindfors AV, Robson TM, Aphalo PJ (2015) Flavonoids in sunlight. Plant Cell Environ 38:941–952

  125. Skaltsa E, Verykokidou E, Harvala C, Karabourniotis G, Manetas Y (1994) UV-B protective potential and flavonoid content of leaf hairs of Quercus ilex. Phytochemistry 37:987–990

  126. Stavrianakou S, Liakopoulos G, Miltiadou D, Markoglou AN, Ziogas BN, Karabourniotis G (2010) Antifungal and antibacterial capacity of extracted material from non-glandular and glandular leaf hairs applied at physiological concentrations. Plant Stress 4(1):25–30

  127. Strack D, Heilemann J, Mömken M, Wray V (1988) Cell wall-conjugated phenolics from Coniferae leaves. Phytochemistry 27:3517–3521

  128. Tattini M, Matteini P, Saracini E, Traversi ML, Giordano C, Agati G (2007) Morphology and biochemistry of non-glandular trichomes in Cistus salvifolius L. leaves growing in extreme habitats of Mediterranean basin. Plant Biol 9:411–419

  129. Tian N, Liu F, Wang P, Yan X, Gao H, Zeng X, Wu G (2018) Overexpression of BraLTP2, a lipid transfer protein of Brassica napus, results in increased trichome density and altered concentration of secondary metabolites. Int J Mol Sci 19:1733

  130. Tozin LRdS, de Melo Silva SC, Rodrigues TM (2016) Non-glandular trichomes in Lamiaceae and Verbenaceae species: morphological and histochemical features indicate more than physical protection. New Zeal J Bot 54(4):446–457

  131. Traw MB, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellins on induction of trichomes in Arabidopsis. Plant Physiol 133:1367–1375

  132. Uphof JCT (1962) Plant hairs. Encycl Plant Anat IV 5:1–206

  133. Václaník T, Beckmann M, Cord AF, Bindewald AM (2017) Effects of UV-B radiation on leaf hair traits of invasive plants—combining historical herbarium records with novel remote sensing data. PLoS ONE 12(4):e0175671

  134. Valkama E, Salminen JP, Koricheva J, Pihlaja K (2004) Changes in leaf trichomes and epicuticular flavonoids during leaf development in three birch taxa. Ann Bot 94(2):233–242

  135. Vermeij GJ (2015) Plants that lead: do some surface features direct enemy traffic on leaves and stems? Biol J Linn Soc 116:288–294

  136. Wagner GJ, Wand E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93(1):3–11

  137. Werker E (2000) Trichome diversity and development. Adv Bot Res 31:1–35

  138. Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297

  139. Wieser G (2002) Ozone. In: R Gasche et al (eds) Trace gas exchange in forest ecosystems. Kluwer Academic Publishers, New York, pp 211–226

  140. Xiao K, Mao X, Lin Y, Xu H, Zhu Y, Cai Q, Xie H, Zhang J (2017) Trichome, a functional diversity phenotype in plant. Mol Biol 6:183

  141. Yamasaki S, Murakami Y (2014) Continuous UV-B irradiation induces endoreduplication and trichome formation in cotyledons, and reduces epidermal cell division and expansion in the first leaves of pumpkin seedlings (Cucurbita maxima Duch. × C. moschata Duch.). Environ Control Biol 52:203–209

  142. Yamasaki S, Noguchi N, Mimaki K (2007) Continuous UV-B irradiation induces morphological changes and the accumulation of polyphenolic compounds on the surface of cucumber cotyledons. J Radiat Res 48:443–454

  143. Yan A, Pan J, An L, Gan Y, Feng H (2012) The responses of trichome mutants to enhanced ultraviolet-B radiation in Arabidopsis thaliana. J Photochem Photobiol B Biol 113:29–35

  144. Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K (2009) Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development 136:1039–1048

  145. Zeiger C, Rodrigues da Silva IC, Mail M, Kavalenka MN, Barthlott W, Hölscher H (2016) Microstructures of superhydrophobic plant leaves—inspiration for efficient oil spill cleanup materials. Bioinspir Biomim 11:056003

  146. Zhang B, Schrader A (2017) TRANSPARENT TESTA GLABRA 1-dependent regulation of flavonoid biosynthesis. Plants 6:65

  147. Zhang T-J, Chow WS, Liu X-T, Zhang P, Liu N, Peng C-L (2016) A magic red coat on the surface of young leaves: anthocyanins distributed in trichome layer protect Castanopsis fissa leaves from photoinhibition. Tree Physiol 36:1296–1306

  148. Zhao F-J, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514

  149. Zhou LH, Liu SB, Wang PF, Lu TJ, Xu F, Genin GM, Pickard BG (2016) The Arabidopsis trichome is an active mechanosensory switch. Plant Cell Environ 40:611–621

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Karabourniotis, G., Liakopoulos, G., Nikolopoulos, D. et al. Protective and defensive roles of non-glandular trichomes against multiple stresses: structure–function coordination. J. For. Res. 31, 1–12 (2020). https://doi.org/10.1007/s11676-019-01034-4

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  • Non-glandular trichomes
  • Phenolics
  • Flavonoids
  • Protection
  • Defence
  • Biotic stress
  • Abiotic stress