Functional interaction between leaf trichomes, leaf wettability and the optical properties of water droplets

Abstract. Because CO₂ diffuses 10000 times more slowly through water than air, there may be strong selective pressure for increased water repellency in terrestrial plant leaves. In the present study, leaf trichomes appeared to have a strong influence on leaf water repellency (i.e. degree of water droplet formation on the leaf surface) as well as the retention of droplets on the leaf. Based upon evaluation of 38 plant species from 21 families, we found that leaves with trichomes were more water repellent, especially where trichome density was greater than 25mm². However, droplet repellency and retention were both high in some species where trichomes entrapped droplets. Finally, the lensing effects of water droplets on leaf surfaces increased incident sunlight by over 20-fold directly beneath individual droplets. These results may have important implications for such processes as stomatal function, whole leaf photosynthesis, and transpiration for a large variety of plant species.     

THE FOLIAR EPIDERMIS IN TILLANDSIOIDEAE (BROMELIACEAE) AND ITS ROLE IN HABITAT SELECTION

Structural features of the foliar epidermal surfaces of selected epiphytic members of subfamily Tillandsioideae of Bromeliaceae were examined to determine why xeromorphic nonimpounding (atmospheric) species with a dense layer of foliar trichomes are seldom found in deeply shaded humid portions of the forest profile, whereas tank-forming members of the same subfamily often abound in such sites. Two features of the peltate trichome which appear to play a major role in enforcing habitat preferences among members of Tillandsioideae are (1) anatomical features of the walls of certain trichome cells which affect the mobility of the shield and. (2) variations in juxtaposition of trichomes and stomates on the leaf surface. Both features are involved in inhibition of gas exchange in wet leaves; trichome shield flexibility is also associated with high leaf reflectivity when the leaf surface is dry.     

Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae)

We examined the relationships between H2O and CO2 gas exchange parameters and leaf trichome cover in 12 species of Tillandsia that exhibit a wide range in trichome size and trichome cover. Previous investigations have hypothesized that trichomes function to enhance boundary layers around Tillandsioid leaves thereby buffering the evaporative demand of the atmosphere and retarding transpirational water loss. Data presented herein suggest that trichome-enhanced boundary layers have negligible effects on Tillandsia gas exchange, as indicated by the lack of statistically significant relationships in regression analyses of gas exchange parameters and trichome cover. We calculated trichome and leaf boundary layer components, and their associated effects on H2O and CO2 gas exchange. The results further indicate trichome-enhanced boundary layers do not significantly reduce transpirational water loss. We conclude that although the trichomes undoubtedly increase the thickness of the boundary layer, the increase due to Tillandsioid trichomes is inconsequential in terms of whole leaf boundary layers, and any associated reduction in transpirational water loss is also negligible within the whole plant gas exchange pathway.     

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

Quartz fibre-optic microprobes were used to monitor the light microenvironment beneath trichome layers of the xeromorphic leaves of two Mediterranean evergreen sclerophylls, Olea europaea and Quercus ilex . Young developing leaves of both plants were densely pubescent on both surfaces of the lamina, whereas the mature leaves were pubescent only on the abaxial side. Trichome layers of young as well as of mature leaves of both plants attenuated almost all incident ultraviolet (UV)-B (310 nm) and UV-A (360 nm) radiation and a considerable portion of blue light (430 nm). Abaxial trichome layers of young leaves were more effective in screening out the incident radiation compared to the adaxial ones of the same leaves and also compared to the abaxial layer of the mature leaves. The abaxial epidermis of dehaired mature leaves of O. europaea was ineffective in absorbing most of the incident UV-B and UV-A radiation. UV and visible spectra beneath trichome layers of O. europaea in mature leaves confirmed that the light microenvironment on the epidermis was deprived in the UV-B, UV-A and partly in the blue spectral regions. It is proposed that the occurrence of a dense trichome layer, especially in young leaves, may play a protective role against not only UV-B radiation damage, but also against high visible irradiance. This function is performed irrespective of the differing anatomy of individual hairs of both plants. The protection provided by the trichomes could afford advantages under stress conditions, especially during leaf development.     

气生凤梨叶片结构研究

我们以地生凤梨(Guzmnania‘Denise’)作为对照,利用扫描电镜技术、石蜡切片技术对3种气生凤梨(Til-landsia stricta‘Hard leaf’、T.stricta‘Cotton candy’与T.filifolia)的叶片表面和内部结构进行了研究。结果表明所有凤梨叶片表面均分布着葵花状的鳞片,鳞片由碟状细胞、环状细胞和翼状细胞3类细胞构成,最内部的碟状细胞通过柄状细胞与叶片内部的叶肉细胞相连。气生凤梨叶片表面鳞片白色、蜡质、密度很大,但气孔很少或不可见,暗示鳞片除吸收水分和养分外,还可能具有减少光呼吸、排水及反射阳光等功能。另外,不同的气生凤梨之间叶片表面鳞片的形态、大小和密度也不同,反映了它们对其不同起源地及现生存环境的适应。     

Leaf hairs influence phytopathogenic fungus infection and confer an increased resistance when expressing a Trichoderma alpha-1,3-glucanase

The leaf surface of a very large number of plant species are covered by trichomes. Non-glandular trichomes are specialized unicellular or multicellular structures that occur in many different plant species and function in xenobiotic detoxification and protecting the plant against pest attack. By analysing the susceptibility of trichome mutants, evidence is provided that indicates the influence of leaf trichomes on foliar fungal infections in Arabidopsis thaliana, probably by facilitating the adhesion of the fungal spores/hyphae to the leaf surface. A decreased trichome number in the hairless Arabidopsis mutant gl1 enhances tolerance against the necrotrophic fungus Botrytis cinerea. By contrast, the try mutant shows an increased susceptibility to both fungal infection and accumulation. Trichome density does not influence infection by the soil-borne pathogen Rhizoctonia solani. In addition, the influence of trichomes on foliar infection is supported by targeting the high-level expression of the Trichoderma harzianum alpha-1,3-glucanase protein to the specialized cell structures. Trichome expression of this anti-fungal hydrolase shows a significant resistance to infection by the foliar pathogen Botrytis cinerea. Resistance to this fungus is not dependent on the constitutive induction of the salicylic or jasmonic defence signalling pathways, but the presence of the alpha-1,3-glucanase protein in trichomes.     

THE ABSORPTIVE CAPACITIES OF BROMELIAD TRICHOMES

Tritiated glycine and leucine and microautoradiographic techniques were employed to determine whether various bromeliad species produce foliar trichomes capable of absorbing these two solutes from solutions placed on intact leaf surfaces. All trichomes borne by members of subfamily Tillandsioideae, whether on the leaf blade or sheath, accumulated both amino acids in substantial quantities. Trichomes located on the leaf sheaths of tank-forming members of Bromelioideae absorbed much smaller quantities while trichomes located on the blades of the same tank-producing bromelioids, as well as those of nontank-forming members of Pitcairnioideae and Bromelioideae, took up little or none at all. The evolution of the bromeliad trichome is considered in the light of these results.     

ABSORBING TRICHOMES IN THE PLEUROTHALLIDINAE (ORCHIDACEAE)

Glandular trichomes occur on both surfaces of leaves of all examined genera and species of the subtribe Pleurothallidinae (Orchidaceae). Trichome initiation is effected by one periclinal division of a protodermal cell, producing a thin-walled, globose apical cell with a relatively large nucleus and a subapical stalk cell with heavily cutinized lateral walls. In some species a second periclinal division produces a third small basal cell also having thick lateral walls but thin transverse walls. As leaf development proceeds, the trichome apparatus assumes a sunken position due to continued anticlinal divisions of protoderm. Prior to laminar expansion and guard-mother-cell division on the abaxial surface, the wall of the apical cell ruptures and is replaced by a brown opaque residue. Finally, after vascular tissue differentiation and the cessation of meristematic activity, two or more pitted foot cells develop at the base of the trichome and adjacent to the water-storing hypodermal layers. Preliminary investigations indicate that the trichome apparatus is absorptive throughout its development and similar in function to tillandsioid scales in Bromeliaceae.     

PATTERNS OF VARIATION IN FOLIAR TRICHOMES OF EASTERN NORTH AMERICAN QUERCUS

Scanning electron microscopy of leaf trichomes of the forty two native species of oaks in eastern North America indicates five patterns of variability: 1) Eight trichome types are evident among the species and each species possesses a definite complement of trichome types. Certain trichomes are restricted to particular subgenera and series. 2) An obvious seasonal loss of trichomes occurs during leaf maturation. This loss may be both quantitative in terms of trichome density and qualitative in terms of trichome type. 3) There is an obvious difference between the adaxial and abaxial surfaces. The adaxial side of most oak leaves is dark green, lustrous, and glabrous or glabrate. The abaxial surface either remains pubescent, becomes glabrate or glabrous, or maintains trichomes along the midrib or in the axils of major secondary veins. There are also initial quantitative and qualitative trichome differences between the two sides. 4) Geographical and ecological variations are due in part to non-genetic ecophenic modifications, ecotypic differentiation, and random genetic differences not necessarily correlated with environmental conditions. Trichome types are considered to be less affected by environment than is trichome density. 5) Hybridization and introgression within a subgenus leads to localized variability. Trichomes of hybrids are usually a combination of the parental types. These five patterns of variation are predictable and appear to be held within rather narrow limits. The complement of foliar trichomes, therefore, is a reliable character in the taxonomy of the oaks.     

Erinea formation on Quercus ilex leaves: anatomical, physiological and chemical responses of leaf trichomes against mite attack

Structures on the surfaces of leaves, such as dense layers of non-glandular trichomes, strongly affect phylloplane mite activities. On the other hand the feeding of eriophyoid mites on leaf surfaces can cause hyperplasia of leaf trichomes (erinea formation). In many cases the hyperplasia is accompanied by the accumulation of pigments within trichome cells, causing an impressive red-brown colouration of the erineum. There is no information, however, on the structure of these pigments as well as on the chemical alterations in the phenolic content of plant trichomes in response to mite attack. Erinea formation on the abaxial surface of Quercus ilex leaves upon Aceria ilicis (Acari: Eriophyoidea) attack provides an excellent model on this topic. Differences in the structure and chemical composition of isolated trichomes derived either from healthy (normal trichomes) or mite attacked (hypertrophic trichomes) leaves were examined. Carbon investment was comparable between the two different trichome types, but the cell walls of the hypertrophic trichomes appeared thinner and did not contain microcrystalline cellulose. Observations under the fluorescence microscope showed that the emitted fluorescence was different between the two trichome types, indicating a different composition in fluorescencing phenolic compounds. The chemical analyses confirmed that hypertrophic trichomes contained higher concentrations of the feeding deterrents proanthocyanidin B3 and catechin, as well as of quercetin-3-O-glucoside, but lower concentrations of acylated flavonoid glycosides, than the normal ones. The results showed that the structural and functional changes in leaf trichomes upon mite attack may be an effort of the leaf to compensate the damage caused by the pest.     

Trichome layers versus dehaired lamina of Olea europaea leaves: differences in flavonoid distribution,UV-absorbing capacity,and wax yield

Leaf flavonoid compounds from six olive (Olea europaea L.) cultivars were analysed by HPLC. The composition of the soluble fractions of the dehaired lamina and the isolated trichome layers of the abaxial leaf surface were analysed in separate, as to study the distribution of flavonoids between the two leaf parts. Quercetin and quercetin 3-O-rhamnoside that have been reported to occur in the leaves seem to be located exclusively in the trichome layer. A greater variety of flavonoids was found in the lamina but the trichome layer was richer in terms of total flavonoids per unit mass. Trichome layer demonstrated an independent chemical character since its flavonoid concentration and composition was not coordinated with that of the lamina. The occurrence of flavonoid compounds in trichomes is related to the UV-filtering capacity of these cells. The results of the present study showed that apart from the soluble fraction, the cuticular waxes and cell walls of the trichomes also showed significant UV-absorbing capacity, indicating the occurrence of UV-absorbing compounds in these fractions as well. Moreover, the cuticular waxes of the trichome layer exhibited not only a higher investment of mass per unit of leaf area, but also a higher UV-absorbing capacity expressed per unit mass as compared to the cuticular waxes of the lamina surface. The importance for the separate chemical investigation of the phenolic composition of the leaf lamina and the trichome layers as well as the ecological significance of the findings is discussed.     

The ultrastructure of the development of Tillandsia (Bromeliaceae) trichome

Tillandsia spp. (Bromeliaceae) use their epidermal trichomes for absorbing atmospheric water, mineral and organic nutrients. The absorbing trichome in Tillandsia has a nail-like shape, formed by an axis (stem) connected to the internal tissues of the leaf, and by an external shield. Water and aqueous liquids coming from the external environment go through the shield cells and then run through the stem, finally reaching the underlying mesophyll parenchyma along a symplastic route.     

Foliar secretory trichomes of Ocimum obovatum (Lamiaceae): micromorphological structure and histochemistry

This study characterises the micromorphology, ultrastructure and main chemical constituents of the foliar glandular trichomes of Ocimum obovatum using light and electron microscopy and a variety of histochemical tests. Two types of glandular trichomes occur on the leaves: large peltate and small capitate. The head of each peltate trichome is made up of four broad head cells in one layer. The head of each capitate trichome is composed of two broad head cells in one layer (type I) or a single oval head cell (type II, rare). In peltate heads, secretory materials are gradually transported to the subcuticular space via fracture in the four sutures at the connecting walls of the head cells. Release to the head periphery occurs through opposite fracture in the four sutures in the head cuticle. In type I capitate trichomes, release of the secretions to the subcuticular space occurs via a pore between the two head cells, and release to the head periphery occurs through the opposite pore in the head cuticle. In type II capitate trichomes, the secreted material is released from the head cell through a ruptured particular squared area at the central part of the head cuticle. These secretion modes are reported for the first time in the family Lamiaceae. Histochemical tests showed that the secretory materials in the glandular trichomes are mainly essential oils, lipophilic substances and polysaccharides. Large peltate trichomes contain a large quantity of these substances than the small capitate trichomes. Ultrastructural evidence suggests that the plastids produce numerous lipid droplets, and the numerous polysaccharide small vesicles are derived from Golgi bodies.     

Effects of induced water stress on leaf trichome density and foliar nutrients of three elm (Ulmus) species: implications for resistance to the elm leaf beetle

Seedlings of three elm species with variable susceptibility to the elm leaf beetle (Pyrrhalta luteola Müller) (Coleoptera: Chrysomelidae) were subjected to three water stress treatments (no stress, low stress, and high stress) in a greenhouse experiment. The species tested were Ulmus pumila L. (Siberian elm = highly susceptible), U. parvifolia Jacq. (Chinese elm = resistant), and U. americana L. (American elm = intermediate). The seedlings were analyzed for changes in the levels of selected host traits (trichome density, foliar concentration of nitrogen [N], phosphorus [P], potassium [K], calcium [Ca], magnesium [Mg], iron [Fe], and manganese [Mn]), some of which had previously been implicated in resistance to the elm leaf beetle. Density of leaf abaxial surface trichomes (simple, bulbous, and total trichomes) and foliar Fe and Mg concentrations increased significantly in the highly susceptible Siberian elms under water stress. In contrast, stress reduced trichome density in the moderately susceptible American elms, but it had no effect on levels of foliar mineral nutrients. The stress treatments had no influence on host traits in the resistant Chinese elms. The results suggest that environmental stress can alter plant traits that are likely involved in determining resistance of elms to the elm leaf beetle.     

Physiological ecology of the Bromeliaceae

The physiological ecology of members of the Bromeliaceae is reviewed with an emphasis on photosynthesis and water relations. Terrestrial and epiphytic species are, for the most part, treated separately. Water relations, photosynthetic pathways, and photosynthetic responses to light, temperature, drought, atmospheric moisture, elemental nutrients, and pollutants are considered from an ecological perspective. In addition, appendices provide values of numerous ecophysiological parameters for all species studied thus far. Results of this review include the following: (1) the ecophysiology of terrestrial and epiphytic species is surprisingly similar; (2) approximately two-thirds of bromeliads are CAM plants and occupy arid sites or are epiphytic; (3) many species are adapted to full or partial shade, yet can grow in full sunlight; (4) photosynthesis is optimal when day temperatures are warm and night temperatures are cool; (5) species with heavy trichome indumenta on their leaf surfaces are capable of absorbing atmospheric water vapor, yet improvement of tissue water relations is unlikely; (6) heavy trichome covers also suppress CO₂ exchange when leaf surfaces are wetted; (7) high levels of recycling of respiratory CO₂ via CAM occur in many species, especially under stress; and (8) tissue osmotic and water potentials of nearly all bromeliads investigated are seldom more negative than -1.0 MPa. A potential explanation of the mechanisms underlying maintenance of high tissue water potentials despite large water losses during droughts is discussed. In summary, the diversity of physiological adaptations to the environment in the few bromeliads studied thus far is impressive, but likely will be surpassed with investigation of more species in the Bromeliaceae.     

Modelled influences of non-exchanging trichomes on leaf boundary layers and gas exchange

The two main resistances in the exchange of gases between plants and the atmosphere are stomatal and boundary layer resistances. We modeled boundary layer dynamics over glabrous and pubescent leaves (assuming non-exchanging trichomes) with leaf lengths varying from 0.01 to 0.2 m, and windspeeds of 0.1-5.0 m x s(-1). Results from theoretical and semi-empirical formulae were compared. As expected, boundary layer thickness decreased with decreasing leaf length and increasing windspeed. The presence of trichomes increased leaf surface roughness, resulting in lowered Reynolds numbers at which the boundary layer became turbulent. This effect is especially important at low windspeeds and over small leaves, where the Reynolds number over glabrous surfaces would be low. We derived a new simple dimensionless number, the trip factor, to distinguish field conditions that would lead to a turbulent boundary layer based on the influence of trichomes. Because modeled rates of CO2 and H2O(v) exchange over turbulent boundary layers are one or more orders of magnitude faster than over laminar boundary layers, a turbulent boundary layer may lead to increased carbon uptake by plants. The biological trade-off is potentially increased transpirational water loss. However, in understory habitats characterized by low windspeeds, even a few trichomes may increase turbulence in the boundary layer, thus facilitating photosynthetic gas exchange. Preliminary field data show that critical trip factors are exceeded for several plant species, both in understory and open habitats.     

Oviposition,larval survival and leaf damage by the willow leaf blotch miner,Micrurapteryx salicifoliella,in relation to leaf trichomes across 10 Salix species

1. Foliar trichomes clearly reduce chewing damage and efficiency of movement by some insect herbivores, but the effect of trichomes on insect oviposition is less well characterised. Trichomes are likely to have particularly strong, negative effects on species that require secure attachment of the egg to the leaf epidermis for successful transition to the feeding stage – a group that includes many leaf mining insects. 2. One such species, Micrurapteryx salicifoliella, must initially enter leaf cells directly from an egg adhered to the cuticle, but later instars can move between leaves and initiate new mines from the leaf exterior. 3. Natural patterns of occurrence by M. salicifoliella were quantified on 10 sympatric Salix species varying in trichome expression to test whether trichomes were associated with reduced oviposition, larval survival and leaf damage. 4. Mean egg density and leaf mining damage were negatively related to mean trichome density across Salix species. Survival of M. salicifoliella from egg to pupa was positively related to trichome density, suggesting that initiation of new mines by late‐instar larvae was not adversely affected by trichomes. There was no evidence that trichomes benefited leaf miner larvae indirectly by decreasing density‐dependent mortality; rather, the positive relationship between trichome density and larval survival may reflect less effective chemical defence by Salix species expressing high trichome density. 5. The results suggest that foliar trichomes serve as an effective defence against M. salicifoliella by deterring oviposition, but do not reduce the survivorship of those individuals that successfully transition from egg to larva.     

Characterization and density of trichomes on three common bean cultivars

Trichomes have been implicated as a mechanism which can confer resistance to both plant pests and drought. A study was conducted to provide information regarding genetic variability for trichome distribution and density among three diverse dry bean (Phaseolus vulgaris L.) cultivars, and to characterize the types of trichomes present among the cultivars. Trichomes on the leaf surfaces were micrographed with a scanning electron microscope (SEM) and counted using a stereomicroscope on both the abaxial and adaxial leaf surfaces of the cultivars ‘Bill Z’, ‘Pompadour Checa’ and ‘Diacol Calima’. Straight, hooked, and glandular trichomes were observed on the leaf surfaces of each cultivar. SEM micrographs are presented for the leaf surfaces of each cultivar and trichome type. The abaxial leaf surface had more straight trichomes than the adaxial leaf surface for ‘Pompadour Checa’ and ‘Diacol Calima’, however ‘Bill Z’ had more on the adaxial surface. The opposite relationship existed among the cultivars and leaf surfaces for the hooked trichomes.     

Environmental Heterogeneity and Population Differentiation in Plasticity to Drought in <Emphasis Type="Italic">Convolvulus Chilensis</Emphasis> (Convolvulaceae)

Plant populations may show differentiation in phenotypic plasticity, and theory predicts that greater levels of environmental heterogeneity should select for higher magnitudes of phenotypic plasticity. We evaluated phenotypic responses to reduced soil moisture in plants of Convolvulus chilensis grown in a greenhouse from seeds collected in three natural populations that differ in environmental heterogeneity (precipitation regime). Among several morphological and ecophysiological traits evaluated, only four traits showed differentiation among populations in plasticity to soil moisture: leaf area, leaf shape, leaf area ratio (LAR), and foliar trichome density. In all of these traits plasticity to drought was greatest in plants from the population with the highest interannual variation in precipitation. We further tested the adaptive nature of these plastic responses by evaluating the relationship between phenotypic traits and total biomass, as a proxy for plant fitness, in the low water environment. Foliar trichome density appears to be the only trait that shows adaptive patterns of plasticity to drought. Plants from populations showing plasticity had higher trichome density when growing in soils with reduced moisture, and foliar trichome density was positively associated with total biomass. Co-ordinating editor: F. Stuefer     

The foliar trichomes of Hypoestes aristata (Vahl) Sol. ex Roem. & Schult var aristata (Acanthaceae) a widespread medicinal plant species in tropical sub-Saharan Africa: with comments on its possible phylogenetic significance

The micromorphology of foliar trichomes of Hypoestes aristata var. aristata was studied using stereo, light and scanning microscopy (SEM). This genus belongs to the advanced angiosperm family Acanthaceae, for which few micromorphological leaf studies exist. Results revealed both glandular and non-glandular trichomes, the latter being more abundant on leaf veins, particularly on the abaxial surface of very young leaves. With leaf maturity, the density of non-glandular trichomes decreased. Glandular trichomes were rare and of two types: long-stalked capitate and globose-like peltate trichomes. Capitate trichomes were observed only on the abaxial leaf surface, while peltate trichomes were distributed on both adaxial and abaxial leaf surfaces.