Foliar Water Uptake in Trees: Negligible or Necessary?

TRPLSC 1920 No. of Pages 14

Trends in Plant Science

Review

Foliar Water Uptake in Trees: Negligible or Necessary? Jeroen D.M. Schreel

1,

* and Kathy Steppe1,*

Foliar water uptake (FWU) has been identified as a mechanism commonly used by trees and other plants originating from various biomes. However, many questions regarding the pathways and the implications of FWU remain, including its ability to mitigate climate change-driven drought. Therefore, answering these questions is of primary importance to adequately address and comprehend drought stress responses and associated growth. In this review, we discuss the occurrence, pathways, and consequences of FWU, with a focus predominantly on tree species. Subsequently, we highlight the tight coupling between FWU and foliar fertilizer applications, discuss FWU in a changing climate, and conclude with the importance of including FWU in mechanistic vegetation models.

Highlights

Occurrence of FWU

As the number of climate changeinduced drought events increases, so too will the relative importance of FWU.

Foliar water uptake (FWU) has been identified as a mechanism commonly used by plants originating from a range of biomes. FWU can rehydrate tissues and result in turgor-driven growth. FWU and the absorption of foliar fertilizers are interlinked, making FWU research important for both natural and agricultural ecosystems.

Incidence and Importance Historically, the ecological importance of FWU has erroneously been neglected (Box 1) because FWU was assumed to be restricted to leaf-wetting events [1,2]. However, neither a saturated atmosphere nor dew point temperature of the leaf surface are critical for FWU to occur. Only a water source and a favorable water potential (see Glossary) gradient are required [3] to drive this reverse flow [4].

Future models should include FWU to correctly assess the impact of climate change on tree growth.

Recent research has indicated that, on average, precipitation inputs leading to leaf-wetting events occur over 100 days per year across all ecoregions of the world [5]. This makes FWU a potential mechanism occurring on a regular basis across biomes. Although the general importance of FWU is increasingly being assessed (e.g., [5,6]), its role under a changing climate is still unclear. Biophysical Background According to the cohesion–tension theory, liquid water transport within trees is driven by transpiration at the leaf level [7]. In this theory, liquid water flows from the soil to the roots through the stem, evaporates in the substomatal cavity, and dissipates as water vapor into the atmosphere through the stomata of the leaves [8,9]. This transport is labeled as the traditional water flow within the soil–plant–atmosphere continuum (SPAC) [10]. Ascent of sap in the SPAC comes to a halt when Ψroot (MPa) drops below Ψleaf (MPa) and is reversed by hydraulic redistribution of liquid water towards drier regions within the plant [11]. The magnitude of transpiration (T; g.h–1) at the leaf level can be expressed by the ratio of the difference in water potential between leaf and atmosphere (ΔΨleaf-atm; MPa) to the gaseous resistance in the transpirational pathway (RT; MPa.h.g–1) as described by van den Honert [12] (Equation 1): T¼

ΔΨleaf−atm RT

1

Laboratory of Plant Ecology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, 9000 Gent, Belgium

½1 –1

In case of FWU (g.h ), water can enter the leaf in three distinct ways: (i) liquid water from precipitation can be absorbed; (ii) water vapor from the atmosphere can condense on the leaf to form Trends in Plant Science, Month 2020, Vol. xx, No. xx

*Correspondence: [email protected] (J.D.M. Schreel) and [email protected] (K. Steppe).

https://doi.org/10.1016/j.tplants.2020.01.003 © 2020 Published by Elsevier Ltd.

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Box 1. History of FWU Research FWU has puzzled researchers for over 300 years, starting with the first report of FWU in 1676 (Paris) [94]. Follow-up research has been conducted in waves as a result of questions regarding the ecological significance of this plant mechanism [95]. Around 1880, it was concluded and proven that FWU occurred to complement water taken up by the roots [94,95]. It took another 40 years to prove that abaxial leaf surfaces generally absorbed water more rapidly compared with the adaxial leaf surface for an unknown, nonstomatal reason [96]. In addition, leaves having a waxy bloom or a dense covering of hairs were labeled as unable to take up water [95,96]. Around 1930, it was concluded that differences in the amount and rate of water absorbed by FWU resulted from internal leaf structure, ease of water conduction away from the leaf towards other organs, and the general degree of tissue hydration [96]. Once these driving factors were obtained, the hydraulic redistribution within the plant of water taken up by leaves was investigated [94]. In 1950, it was stated that tomato plants could take up water through their leaves and exude it back through the roots into the surrounding soil [97], thus indicating a reverse water movement throughout the entire plant [48]. Simultaneously, a relatively rapid consensus was reached about the reduction in transpiration due to water covering the leaves, which resulted in stomatal closure. This also led to the assumption that the duration of leaf wetness is of primary importance, by contrast to the total amount of water supplied [94]. This assumption is based on the fact that water enters leaves slowly and, as such, is a function of time rather than of the amount applied [94]. This hypothesis has recently been confirmed [57]. After the 1960s, FWU research stagnated for a few decades, resulting in only a handful of research papers between that time and 1990. During the 1990s, the most recent wave of FWU research started and remains ongoing.

liquid water and be absorbed; or (iii) water vapor can enter the substomatal cavity, where it condenses into liquid water and is absorbed. Absorbed water goes to or through the plant and possibly into the soil, resulting in a complete reversal of the traditional SPAC flow [2,13]. In general, FWU can be described by Equation 2 [14–16], FWU ¼ ΔΨleaf−atm :kFWU

½2

with kFWU (g. MPa-1.h–1) representing the hydraulic conductance from atmosphere to leaves. As such, T and FWU are both driven by ΔΨleaf-atm and can be described by the same basic concept. However, RT and kFWU in Equation 1 and Equation 2, respectively, are not each other’s inverse because T is driven by the diffusion of water vapor through the stomata, whereas FWU is driven by diffusion through the cuticle [17] or absorption by stomatal pores [18], trichomes [19], or hydathodes [20] (see Outstanding Questions and the ‘Morphological and Anatomical Structures’ section). It has been suggested that reverse transpiration through stomata accounts for most of the water absorbed by FWU, indicating that RT and the inverse of kFWU have the same order of magnitude [16]; however, more research is needed to substantiate these claims. Sap flow from roots to the atmosphere, and vice versa, are illustrated in Figure 1 and can be described by Equations 3 and 4.

where Ψroot–atm (MPa), Ψroot–stem (MPa), and Ψstem–leaf (MPa) are the difference in water potential between roots and atmosphere, roots and stem, and stem and leaves, respectively. Rroot–atm (MPa.h.g–1), Rr (MPa.h.g–1), and Rst (MPa.h.g–1) represent the hydraulic resistance for water flow from roots to atmosphere, roots to stem, and stem to leaves, respectively. 2

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Glossary Cuticle: a waxy layer covering the epidermal cells of leaves. Foliar fertilizer (FF): liquid fertilizers that are applied to leaves. Foliar water uptake (FWU): absorption of water by leaves, resulting in a net increase in leaf water content. Hydathode: a pore at the leaf margin, capable of secreting water. Hydraulic redistribution: redistribution of water within the plant. Mechanistic tree model: a tree model based on physical equations of water flow and storage within different compartments of the tree. Stomata: small pores at the leaf surface that allow gas exchange. Transpiration: evaporation of water vapor from the leaf interior through the stomata towards the atmosphere. Trichomes: here, fine epidermal outgrowths or ‘hairs’, on leaves. Water potential (Ψ): a measure of free energy of water per unit of volume in a compartment (i.e., a direct measure of water status).

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(See figure legend at the bottom of the next page.)

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Only when liquid water comes into contact with leaves, and leaves have a low water potential, (e.g., due to limited soil water availability, height, or increased hydraulic resistance), a substantial FWU is likely to occur [2,4,15]. As such, four ecophysiological criteria have been formulated by Rundel [3] to define FWU: (i) a gradient of decreasing Ψ from atmosphere to plant must be present; (ii) morphological or anatomical structures facilitating water uptake must be present; (iii) significant amounts of water must be taken up and redistributed within the plant; and (iv) Ψplant must increase significantly as a direct effect of FWU. FWU has been confirmed for an increasing number of plant species (Table 1), both trees and other plants, from a range of different climate types, based on a variety of measurement methods (see also Box S1 in the supplemental information online). However, some of these measurement methods fail to distinguish between FWU and stem or bark water uptake (SWU) [21]. Given that SWU was recently reported to result in embolism repair [21,22] and general hydraulic recovery [23], it is essential to separate these two phenomena when assessing their respective physiological importance and relative contribution. Our meta-analysis identifies over 180 species that are capable of FWU, representing ~93% of all studied species (see also Table S1 in the supplemental information online). However, it is more probable for positive data to get published compared with negative results. As such, the percentage of species capable of FWU might be skewed, leading to an overestimation of the calculated percentage (Table 1). In general, the importance of this mechanism varies significantly between different species [24], between different specimens from the same species [25], and throughout the different life stages of the same species [26]. FWU is assumed to be of primary importance for seedlings and trees with limited access to soil water [2], such as trees growing in forests with steep slopes [11], saline conditions [27], and for shallow-rooting species [28]. Given that FWU frequently occurs across biomes, questions regarding the entering pathway of water in leaves and its implications are pressing.

Influx Hypotheses Morphological and Anatomical Structures Even though research regarding the pathways used for FWU has increased [5], this route is poorly understood for most species [29,30], giving voice to several different entering hypotheses, such as diffusion based on cuticle permeability [17] or absorption by stomatal pores [18] (indicated as reverse transpiration when assessing water vapor [31]) trichomes [19], or hydathodes [20] (Figure 2). Diffusion of water through the cuticle depends on cuticular wettability and permeability [32]. Cuticle hydrophobicity has been shown to decrease due to regular fogging, resulting in a more wettable and permeable cuticle [1,33,34]. This might be the result of a hypothesized ‘dynamic aqueous continuum’, indicating that aqueous connections or pores are formed in the cuticle during high relative humidity events as a result of cuticular swelling [32]. These pores disappear again during low relative humidity, making them distinctly different from tube-like aquaporins [32]. It is speculated that an increased leaf hydrophobicity in dry environments might be favorable to increase soil water availability from small precipitation events by leaf dripping [33], making these Figure 1. Electrical Analogon Diagram for Sap Flow Resulting from Transpiration (T) and Foliar Water Uptake (FWU) in a Tree (Framed by a Broken Line) (Internal Water Storage not Considered). The water potential of the soil, roots, stem, leaves, and atmosphere is represented by Ψsoil, Ψroot, Ψstem, Ψleaf, and Ψatm, respectively. The hydraulic resistance for the flow from soil to root, from root to stem, from stem to leaves, and from leaves to atmosphere (i.e., transpiration) is given by Rso, Rr, Rst, and RT, respectively. The hydraulic conductance from the atmosphere to the leaves (i.e., FWU) is given by kFWU.

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Table 1. Percentage of Species Capable of FWU as a Function of Climatic Variables Variablea

Subvariablea

Percentage of species capable of FWU±SE

Number of observed species

Main climate

Arid

71±11

17

Equatorial

100

48

Snow

100

38

Warm temperate

92±3

83

Cold arid

100

3

Cool summer

100

4

Temperature

Precipitation

a

Hot arid

64±13

14

Hot summer

90±5

40

Warm summer

96±2

77

Desert

64±13

14

Fully humid

100

54

Monsoonal

100

33

Steppe

100

3

Summer dry

82 ± 6

39

Winter dry

100

43

Based on the Köppen–Geiger classification.

leaves less responsive to FWU. Although previous studies have found no direct link between leaf hydrophobicity and FWU [34], all species in our meta-analysis incapable of performing FWU originated from environments with a dry summer (Table 1). These results suggest that leaf

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Figure 2. Schematic of the Four Most Commonly Accepted Influx Hypotheses for Foliar Water Uptake (FWU). Different leaf structures could aid in FWU. Liquid water can either diffuse through the cuticle or be absorbed by trichomes, hydathodes, or stomata. Water vapor can diffuse through stomata from the atmosphere to the leaf interior, a process indicated as reverse transpiration.

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hydrophobicity and FWU are interlinked. Furthermore, it must be kept in mind that the physical structure [32] and chemical composition of the cuticle cannot be neglected when assessing this pathway for FWU [35]. Stomata have the longest running ‘relation’ with FWU and have historically shifted from the most probable pathway, to unable to absorb water due to the formation of water droplets, back to one of the four most accepted pathways for FWU [32]. One of the main reasons for the reinstatement of stomata as a possible contributor to FWU is the possibility that they are ‘activated’ by the formation of a continuous thin (assumed 100 nm or less) water film connecting the apoplast with the leaf surface (hydraulic activation of stomata, HAS) [36]. HAS can occur as a result of fungal hyphae [29,36], epistomatal mucilage plugs [36,37], and hygroscopic aerosols, often salts [18,36], ranging from metals to sodium, calcium, and magnesium [18]. When the deliquescence relative humidity is reached, hygroscopic aerosols form a liquid solution [32], thus developing a thin water film on the leaf surface and resulting in a bidirectional transport of water and solutes between the leaf surface and leaf interior [36]. Deliquescence relative humidity values are highly variable and depend on the chemical composition of the occurring aerosols [32]. When assessing the trichome hypothesis, it should be noted that a large variety of trichomes exist (e.g., glandular and nonglandular, and hair- or scale-like), with the possible cooccurrence of different types of trichome on the same leaf, each with a different functionality towards FWU. It has been shown that the reduction in transpirational water loss due to a trichome-induced boundary layer can be negligible [38], making the facilitating effect of a trichome induced-boundary layer on FWU (i.e., reverse transpiration) improbable. By contrast, scar tissue resulting from shedding of trichomes has been reported to contribute to water uptake [39]. While trichomes of some species appear to decrease the retention of liquid water, trichomes of other species are able to increase retention and enhance leaf wetness [40], making trichome functionality very species dependent. It is assumed that the ability of a species to exude water through hydathodes in well-watered conditions (i.e., guttation) is correlated with their ability to absorb water by FWU [20]. This hypothesis is based on research by Martin and von Willert [20]. These authors applied nocturnal misting to Crassula spp. and concluded that an increase in leaf thickness after nocturnal misting indicated FWU by hydathodes. However, Crassula spp. use crassulacean acid metabolism (CAM), indicating that they open their stomata during nighttime. As such, nocturnal opening of stomata might have affected the FWU measurements. This hypothesis is reinforced by studies indicating that CAM cycling might not only conserve water, but possibly also aid in nocturnal water absorption [41]. It has been stated that different species use different pathways for FWU [1]. Despite recent research confirming the co-occurrence of multiple pathways in the same species [42], this co-occurrence and the possibility that different species use the same multiple pathways in different proportions has been insufficiently investigated and emphasized (see Outstanding Questions). For example, when dehydrated leaves take up water through trichomes or hydathodes, Ψleaf increases, leading to an increase in cell turgor according to the Höfler diagram. Due to the mechanical advantage that epidermal cells have over guard cells when water potential is uniformly increased [43], active regulation of the osmotic pressure of guard cells is necessary to overcome this mechanical advantage and to cause the stomatal aperture to increase. When the stomatal aperture does increase due to the combination of an elevated water potential and osmotic regulation, the stomata become more prone to FWU. 6

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The Age Effect Changes in foliar anatomy and morphology according to plant developmental stage (i.e., heteroblasty) have been reported for several tree species. Some of these changes include a decreasing trend in individual leaf area and an increase in cuticular thickness with increasing tree size and age [44]. When focusing on individual leaves rather than whole-plant individuals, younger leaves appear to have a more hydrophobic cuticle, thus limiting FWU [45]. Once hygroscopic particles start to accumulate, hydrophobicity is partly lost and FWU through stomata becomes more probable through HAS [18]. However, some leaves are water repellent due to surface roughness and the presence of hydrophobic waxes. This leads to an increased contact angle resulting in the removal of surface particles by down-flowing precipitation, fog, or dew [46,47]. These waxy layers can erode due to mechanical abrasion or rain. Small erosive effects can be regenerated, whereas larger erosive effects cannot, possibly reversing the water-repellent characteristics and making the leaf more wettable [47]. This might explain why old leaves appear to be better suited for FWU of fog [29].

Implications of FWU Hydraulic Redistribution of Foliar Absorbed Water In accordance with the cohesion–tension theory, liquid water flows from soil to roots, stem, and leaves, as a result of transpiration [7] (Figure 3A). When leaves absorb water during a rainfall event, their water potential increases, favoring rehydration of tissues and organs closest to the point of uptake [29], and eventually resulting in a bidirectional flow from leaves and roots towards stem (Figure 3B). During leaf-wetting events, a small increase in soil water potential can occur, while large increases in soil water potential can be hindered (e.g., due to canopy interception of long, but mild, precipitation events). When a rainfall event persists for a longer period of time, the water reserves of the stem are replenished and the water potential of the stem rises above the water potential of the roots, resulting in a bidirectional flow from the stem and the soil towards the roots (Figure 3C). When rainfall persists even longer, a complete reversal of the flow can

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Figure 3. Changes in Flow Direction and Water Potential (Values Are Illustrative) as a Result of Foliar Water Uptake (FWU). (A) Flow before any rain event from soil to leaves. (B) Flow at the start of a rainfall event with FWU resulting in bidirectional flow from root and leaves to the stem. (C) Flow after the start of the rainfall event, before complete flow reversal resulting in a bidirectional flow from stem and soil to the roots. (D) Complete flow reversal during a rainfall event resulting in flow from leaves to soil. Adapted from [49].

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occur, resulting in flow from the leaves towards the soil (Figure 3D). It has been found that this water can also be partially used to replenish soil water content [48]. As such, plants could benefit subsequent days after leaf-wetting events by using water transported to the soil. Species incapable of FWU rooting in the vicinity of species capable of FWU could benefit from this process, analogues to shallow-rooting plants using water originating from hydraulic lift caused by deeprooting species [11]. This reverse flow from leaves to stem is continuous and even aided rather than hindered by the gravitational water potential. Therefore, leaf water potential only needs to be slightly higher than soil water potential to result in a complete flow reversal [49]. As tissues rehydrate due to this reverse flow, turgor pressure in living cells increases. When turgor exceeds a critical threshold value Γ (MPa), irreversible growth occurs, as described by Lockhart’s equation (1965) [50] (Equation 5). This equation describes how the relative change ! dV in volume (i.e., growth rate) is driven by the positive hydrostatic pressure (Ψp; MPa) or V:dt turgor when a critical threshold value is exceeded. The proportionality factor between growth rate and this driving factor is defined as cell wall extensibility (ϕ; MPa−1s−1). When water flows into a cell, the cell volume will irreversibly change when cell wall extension takes place [51]. This FWU-induced turgor-driven growth has already been confirmed in the mangrove tree Avicennia marina [27,49] (see Outstanding Questions). 8   dV > > < V:dt ¼ ϕ Ψp −Γ

for Ψp NΓ

> > : dV ¼ 0 V:dt

for Ψp ≤Γ

½5

It has been suggested and indicated that FWU results in embolism repair [21,29,52], both at the branch and leaf level [5]. This would imply that FWU can increase hydraulic conductivity. As such, FWU could partially mitigate the negative effects of drought, such as carbon starvation and hydraulic failure [1]. Although embolism repair has been demonstrated in small plants, such as grapevine (Vitis vinifera), by noninvasive imaging techniques [53], no consensus has yet been reached on the prevailing mechanisms [54]. FWU might be an essential mechanism for embolism repair in tall trees because it is unlikely that the high water potentials needed for hydraulic recovery can be reached in upper canopies of tall trees in the absence of FWU due to gravitational limitations [55,56]. Photosynthetic Implications of FWU Initially, leaf-wetting events could be thought of as detrimental to photosynthesis because the water film reduces the diffusion of CO2 [1]. However, incident radiation is generally low due to clouds during leaf-wetting events, making the expected negative impact on photosynthesis negligible [1]. Additionally, turgor of the stomatal guard cells might improve following FWU (depending on osmotic regulation, see ‘Morphological and Anatomical Structures’ section), resulting in enhanced gas exchange and photosynthesis as soon as more radiation can be intercepted by the leaves. Hence, FWU can decouple leaf-gas exchange from soil water availability, resulting in a positive effect on the plant carbon and water balance when a soil water deficit at root level occurs [1,28,57]. This enables plants to benefit from most precipitation events, even when soil moisture content does not increase substantially [28,58]. Binks et al. [59] recently stated that FWU by Amazonian trees was estimated to result in a carbon assimilation of 2.5 tons per hectare per year, based on an average kFWU. While the effects of kFWU were seasonal, and generally more substantial during drought, these positive effects 8

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equate to N8% of the gross primary production of these trees [59], thus illustrating the potential positive effects of FWU on carbon gain. Link between Foliar Fertilizer and FWU? Spraying foliar fertilizers (FFs) is a widely used practice to correct for nutrient deficiencies, possibly due to unintentional improper application of nutrients to the roots [60,61], and can ameliorate acute leaf deficits. Even more, when applying nutrients by FF, competition with soil-bound bacteria can be reduced, resulting in greater fertilization efficiency [62] and leading to both economical (increase in yield) and ecological (reduced leaching) advantages. Uptake of foliar nitrogen (N) from wet depositions is significantly influenced by the amount of pedospheric N fertilization [63], N form (e.g., urea or nitrate) applied to the leaves, tree species, leaf phenology, and leaf wettability [63–65]. Other limiting factors include the timing of application and leaf age [66]. Except for the amount of pedospheric N fertilization and N form dependency, these are the same factors governing FWU. In fact, a deficiency in pedospheric N affecting FF is the N analog for a water deficiency (i.e., drought) influencing FWU, making N-form dependency the only difference in limiting factors between N FF and FWU. Different pathways have been proposed for FF uptake, such as the use of epidermal trichomes [67], cuticle permeability [68], or stomatal pores [68], indicating that three out of four pathways suggested for FWU also hold for FF. The only pathway that has not been suggested for FF uptake so far is the use of hydathodes, which is also the pathway that has been questioned for FWU uptake in this review. Moisture stress is known to hinder foliar N absorption by an increase in cuticle wax [69]. This effect can be partly mitigated by adding additional surfactant to the FF [69]. These surfactants might also result in HAS, leading to FWU. Given that FF application is in fact spraying a watery solution enriched with nutrients onto the leaves, questions arise as to whether: (i) the improvement in plant health is solely due to FF or also a response to FWU; and (ii) the potential magnitude of FWU in different species corresponds with the potential magnitude of nutrient absorption of FFs (see Outstanding Questions)?

FWU in a Changing Climate Global climate change is predicted to result in changing precipitation patterns, a rise in mean global temperature and an increase in extreme weather events [70]. This has resulted in a global increase in drought frequency and duration [70–75]. This increased number of drought events results in a decreasing number of leaf-wetting events, making FWU a seemingly less important mechanism [76]. However, the impact of drought on FWU is not unidirectional because drought also results in a more negative leaf water potential, which results in more FWU [76] (Equation 2). Despite the fact that the overall effect of drought on FWU remains unclear, the importance of a high relative humidity, morning dew, and small rainfall events ,which do not substantially wet the soil, will increase during these drought events. Survival of the Fittest A trade-off between drought resistance and drought avoidance in relation to the FWU capacity of multiple plant species has been pinpointed, indicating that species with a high FWU capacity tend to have a limited water storage capacity [76,77]. This might explain why these species tend to lose turgor during drought [78] because leaf water storage and FWU can both buffer the leaf water status during drought [6]. However, when addressing drought effects and FWU, some other plant traits, such as drought-mediated shedding of leaves and average leaf life span, should not be overlooked, because FWU can only occur when leaves are present.

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Tree and forest survival under climate change-driven drought has been the topic of intense debate [79–82]. Climate change-induced forest decline reduces cloud occurrence through reductions in transpiration, resulting in decreased cloud water interception and increased evaporative demand, thus reinforcing the negative effects on the hydraulic cycle [28]. This type of forest decline has already been reported in Europe concomitant with tree dieback in Switzerland and the western USA [18]. As such, understanding the different mechanisms underlying individual and interactive tree responses to climate change is of vital for understanding how tree species will be affected by this global phenomenon [83,84]. Due to inter- and intraspecies differences in the magnitude of FWU [24,25], the effects of climate change-driven drought and changes in precipitation patterns will not affect all individual plants and species in a similar way [25] (G.R. Goldsmith, PhD thesis, University of California, Berkeley, 2012). Based on our meta-analysis (Table 1), it can be concluded that the potential of species to absorb water with their leaves is independent of the climatic variable ‘temperature’ because every ‘temperature’ type, or subvariable, has species that either can or cannot use the mechanism of FWU (except for the subvariables with a low number of observations). It appears that FWU is more dependent on the climatic variable ‘precipitation’ because all species unable to absorb water through their leaves originate from the same two subvariables: ‘summer dry’ and ‘desert’. A dry period during the summer might be a prominent driving factor in the evolution of species, making them unable to use the mechanism of FWU if it is not beneficial in the long run due to larger water losses than gains. This also became clear when assessing the evolution of species with reference to FWU, based on the ‘main climatic’ types. In other words, leaves better suited for FWU are more likely to lose water when the water potential gradient is reversed. Timing and Duration of Leaf-Wetting Events Timing of leaf-wetting events, both on a diel and a seasonal scale, determines their ecophysiological importance [5]. When severe drought events prevail, tissue dehydration may occur [11]. As such, FWU may be an important water source for rehydrating plant tissues, reducing the dependency on water in the rootzone, and recharging soil water availability [48]. This soil water recharge may be sufficient to prevent permanent damage to root structures by drought [11] and can increase survival rates [85,86]. Hence, plants can partially decouple their water status from the soil water availability [14] thus improving the entire plant water status [29]. On a daily scale, an important difference exists between daytime and nocturnal leaf-wetting events. A lower vapor pressure deficit (VPD) occurs naturally during nighttime due to a decrease in air temperature. As a result of this reduced VPD, nocturnal stomatal conductance (g; mmol m-2 s-1) in C3 and C4 species can be up to 90% of daytime g, while only leading to transpiration rates of 5–15% compared with daytime [87]. It might be stipulated that nocturnal opening of the stomata occurs to allow water vapor to enter the leaves [24,27]. This would explain why Sequoia sempervirens and other species appear to have poor stomatal control during foggy nights [29,57]. This hypothesis is reinforced by the observations of Caird et al. [87] indicating an increase in stomatal opening during predawn hours when VPDs are low and dew is formed [88]. They additionally observed an increase in daily stomatal opening when nocturnal stomatal opening occurred [87], possibly because of an elevated turgor of the guard cells during the day due to nocturnal FWU, concomitant with an osmotic regulation (see ‘Morphological and Anatomical Structures’ section). Climatic Plasticity Plants can regulate water transport in response to water availability and evaporative demand by varying the stomatal aperture [28], generally resulting in stomatal closure during periods of water 10

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shortage [89]. If FWU occurs through stomata, stomatal closure will reduce the water absorption capacity of leaves. However, if other pathways are used and the conditions for FWU are favorable (e.g., at night when relative humidity increases), some species might survive severe drought events because of FWU. Furthermore, some plants can apply osmotic adaptation to maintain turgor during drought by attracting water taken up by the roots [90]. The resulting reduction in leaf osmotic potential may also improve FWU capacity. Despite first indications of the effects of FWU on a larger scale [59], the impact of FWU on the ecosystem water and carbon balance remains largely unknown [91]. Given that changes at the leaf, whole-plant, and ecosystem level are becoming increasingly apparent, further investigation is needed to assess the relative contribution of FWU on different levels.

Modeling FWU Historically, the ecological importance of FWU has been debated, resulting in its exclusion from ecological, hydrological, atmospheric, and climatological models [58]. However, recent research and opinion papers emphasize the ecological importance of this mechanism in today’s and future climates, making its integration in models more relevant than ever before [92]. Some underlying mechanisms have since been unraveled (Equations 3 and 4), resulting in the first attempt to include FWU in a mechanistic tree model that enables the description of associated turgor-driven radial stem growth spurts based on Lockhart’s equation (Equation 5) [27]. Still many challenges exist, with a predominant importance resting on the inclusion of two potentially different pathways for T and FWU (RT and kFWU in Equations 1 and 2, respectively), and the incorporation of the 3D complexity of leaves [93]. Even though up-scaling of point measurements is challenging due to the large variability in FWU between leaves of different ages and water status [29], a first attempt has been undertaken [59]. Implementing FWU should become the standard to correctly assess the impact of changing rainfall patterns on tree growth [27]. Given that climate change-induced drought events are predicted to increase [70], and the mounting evidence of the relative importance of FWU [92], including FWU in the different types of model (ecological, hydrological, atmospheric, and climatological models) from which it was first omitted, becomes urgent. With new developments in measurement techniques to assess FWU (see also Box S1), our scientific knowledge of the effects of FWU on the water balance of trees is rapidly expanding. This results in increased mechanistic understanding of when, where, how, and to what extent water is absorbed by leaves, increasing the ability of models to correctly represent tree hydraulics at different spatiotemporal scales.

Outstanding Questions Is the pathway used for FWU universal or species specific? Do multiple pathways co-occur in one species? How do the pathways used by FWU affect the hydraulic conductance from atmosphere to leaves (kFWU)? How does the gaseous resistance in the transpirational pathway (RT) differ from the hydraulic resistance for FWU (1/kFWU)? Can the amounts of water absorbed by FWU significantly affect tree growth? Is this effect different or similar in seedlings, saplings, and full-grown trees of the same species? How will dependency on FWU impact the response of trees to climate change? What is the impact of FWU on hydraulic conductivity during drought? Can the link between FWU and FF result in an agricultural shift towards the use of FF away from pedospheric nutrient applications by increasing knowledge of leaf absorption?

Concluding Remarks and Future Perspectives Recent research has identified FWU as a common mechanism used by trees and plants across the world. The predicted, and already observed, increase in the number of drought events highlights the importance of FWU governed by a high relative humidity, morning dew, and small rainfall events that do not substantially wet the soil. The increased water potential difference between leaves and atmosphere during drought potentially increases the relative contribution of FWU; however, a trade-off is made because FWU is more important but occurs less frequently during drought due to a reduced number of leaf-wetting events (see Outstanding Questions). Even though our insight into FWU is rapidly improving, various challenges remain to be tackled: the pathways for FWU are still under debate and should be investigated more in-depth, together with the implications of this absorbed water in general, and more specifically for tree growth and under different climate change scenarios. Given that the importance of FWU is expected to Trends in Plant Science, Month 2020, Vol. xx, No. xx

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increase as climate change progresses, future studies should investigate the interactive effect of FWU and other climate-driven factors, such as drought and variations in relative humidity of the air. In addition, because FWU is predicted to become more important, it should be included in our suite of models ranging from mechanistic tree to ecological, hydrological, atmospheric, and climatological models. These models could result in better predictions of climate changeinduced changes in vegetation cover and, inversely, would help to better assess the full-scale impact of FWU. Lastly, the relationship between FWU and FF application should be investigated in-depth because this might lead to important new insights regarding the best timing and types of FF to be used, featuring both economic and ecological advantages. Acknowledgments This work was supported by the Research Foundation - Flanders (FWO) through a PhD grant to J.D.M.S.

Supplemental Information Supplemental information associated with this article can be found online at https://doi.org/10.1016/j.tplants.2020.01.003.

References 1.

2. 3. 4.

5. 6.

7. 8. 9. 10. 11. 12. 13.

14.

15.

16. 17.

18. 19.

20.

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Eller, C.B. et al. (2013) Foliar uptake of fog water and transport belowground alleviates drought effects in the cloud forest tree species, Drimys brasiliensis (Winteraceae). New Phytol. 199, 151–162 Goldsmith, G.R. (2013) Changing directions: the atmosphereplant-soil continuum. New Phytol. 199, 4–6 Rundel, P.W. (1982) Encyclopedia of Plant Physiology Plant Ecology II Water Relations and Carbon Assimilation, Springer Eller, C.B. et al. (2015) Environmental controls in the water use patterns of a tropical cloud forest tree species, Drimys brasiliensis (Winteraceae). Tree Physiol. 35, 387–399 Dawson, T.E. and Goldsmith, G.R. (2018) The value of wet leaves. New Phytol. 219, 1156–1169 Berry, Z.C. et al. (2019) Foliar water uptake: processes, pathways, and integration into plant water budgets. Plant Cell Environ. 42, 410–423 Dixon, H.H. and Joly, J. (1895) On the ascent of sap. Philos. Trans. R. Soc. London 186, 563–576 Taiz, L. and Zeiger, E. (2002) Plant Physiology, Sinauer Nobel, P.S. (2009) Physicochemical and Environmental Plant Physiology, Academic Press Philip, J.R. (1966) Plant water relations: some physical aspects. Annu. Rev. Plant Physiol. 17, 245–268 Nadezhdina, N. et al. (2010) Trees never rest: the multiple facets of hydraulic redistribution. Ecohydrology 3, 431–444 Van Den Honert, T.H. (1948) Water transport in plants as a catenary process. Discuss. Faraday Soc. 3, 146–153 Cassana, F.F. et al. (2016) Effects of soil water availability on foliar water uptake of Araucaria angustifolia. Plant Soil 399, 147–157 Simonin, K.A. et al. (2009) Fog interception by Sequoia sempervirens (D. Don) crowns decouples physiology from soil water deficit. Plant Cell Environ. 32, 882–892 Oliveira, R.S. et al. (2014) The hydroclimatic and ecophysiological basis of cloud forest distributions under current and projected climates. Ann. Bot. 113, 909–920 Binks, O. et al. (2019) Equivalence of foliar water uptake and stomatal conductance? Plant Cell Environ. 43, 524–528 Ketel, D.H. et al. (1972) Water uptake from foliar-applied drops and its further distribution in the oat leaf. Acta Bot. Neerl. 21, 155–166 Burkhardt, J. (2010) Hygroscopic particles on leaves: nutrients or desiccants? Ecol. Monogr. 80, 369–399 Ohrui, T. et al. (2007) Foliar trichome- and aquaporin-aided water uptake in a drought-resistant epiphyte Tillandsia ionantha Planchon. Planta 227, 47–56 Martin, C.E. and von Willert, D.J. (2000) Leaf epidermal hydathodes and the ecophysiological consequences of foliar water uptake in species of Crassula from the Namib Desert in Southern Africa. Plant Biol. 2, 229–242

Trends in Plant Science, Month 2020, Vol. xx, No. xx

21. Mayr, S. et al. (2014) Uptake of water via branches helps timberline conifers refill embolized xylem in late winter. Plant Physiol. 164, 1731–1740 22. Earles, J.M. et al. (2016) Bark water uptake promotes localized hydraulic recovery in coastal redwood crown. Plant Cell Environ. 39, 320–328 23. Fuenzalida, T.I. et al. (2019) Shoot surface water uptake enables leaf hydraulic recovery in Avicennia marina. New Phytol. 224, 1504–1511 24. Limm, E.B. et al. (2009) Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. Oecologia 161, 449–459 25. Limm, E.B. and Dawson, T.E. (2010) Polystichum munitum (Dryopteridaceae) varies geographically in its capacity to absorb fog water by foliar uptake within the redwood forest ecosystem. Am. J. Bot. 97, 1121–1128 26. Feild, T.S. and Dawson, T.E. (1998) Water sources used by Didymopanax pittieri at different life stages in a tropical cloud forest. Ecology 79, 1448–1452 27. Steppe, K. et al. (2018) Direct uptake of canopy rainwater causes turgor-driven growth spurts in the mangrove Avicennia marina. Tree Physiol. 38, 979–991 28. Tognetti, R. (2015) Trees harvesting the clouds: fog nets threatened by climate change. Tree Physiol. 35, 921–924 29. Burgess, S.S.O. and Dawson, T.E. (2004) The contribution of fog to the water relations of Sequoia sempervirens (D. Don): foliar uptake and prevention of dehydration. Plant Cell Environ. 27, 1023–1034 30. Lambers, H. et al. (2008) Plant Physiological Ecology (2nd edn), Springer 31. Vesala, T. et al. (2017) Effect of leaf water potential on internal humidity and CO 2 dissolution: reverse transpiration and improved water use efficiency under negative pressure. Front. Plant Sci. 8, 1–10 32. Fernández, V. et al. (2017) Physico-chemical properties of plant cuticles and their functional and ecological significance. J. Exp. Bot. 68, 5293–5306 33. Pina, A.L.C.B. et al. (2016) Dew absorption by the leaf trichomes of Combretum leprosum in the Brazilian semiarid region. Funct. Plant Biol. 43, 851–861 34. Goldsmith, G.R. et al. (2017) Variation in leaf wettability traits along a tropical montane elevation gradient. New Phytol. 214, 989–1001 35. Boanares, D. et al. (2018) Pectin and cellulose cell wall composition enables different strategies to leaf water uptake in plants from tropical fog mountain. Plant Physiol. Biochem. 122, 57–64 36. Burkhardt, J. et al. (2012) Stomatal penetration by aqueous solutions - an update involving leaf surface particles. New Phytol. 196, 774–787

Trends in Plant Science

37. Zimmermann, D. et al. (2007) Foliar water supply of tall trees: evidence for mucilage-facilitated moisture uptake from the atmosphere and the impact on pressure bomb measurements. Protoplasma 232, 11–34 38. Benz, B.W. and Martin, C.E. (2006) Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae). J. Plant Physiol. 163, 648–656 39. Fernández, V. et al. (2014) Wettability, polarity, and water absorption of Holm Oak leaves: effect of leaf side and age. Plant Physiol. 166, 168–180 40. Grammatikopoulos, G. and Manetas, Y. (1994) Direct absorption of water by hairy leaves of Phlomis fruticosa and its contribution to drought avoidance. Can. J. Bot. 72, 1805–1811 41. Matimati, I. et al. (2012) Diurnal stem diameter variations show CAM and C3 photosynthetic modes and CAM–C3 switches in arid South African succulent shrubs. Agric. For. Meteorol. 161, 72–79 42. Boanares, D. et al. (2018) Strategies of leaf water uptake based on anatomical traits. Plant Biol. 20, 848–856 43. Buckley, T.N. (2005) The control of stomata by water balance. New Phytol. 168, 275–292 44. Steppe, K. et al. (2011) Tree size- and age-related changes in leaf physiology and their influence on carbon gain. In Size- and Age-Related Changes in Tree Structure and Function (Meinzer, F.C. et al., eds), pp. 245, Springer 45. Cape, J.N. (1983) Contact angles of water droplets on needles of Scots Pine (Pinus sylvestris) growing in polluted atmospheres. New Phytol. 93, 293–299 46. Barthlott, W. and Neinhuis, C. (1997) Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202, 1–8 47. Neinhuis, C. and Barthlott, W. (1997) Characterization and distribution of water-repellent, self-cleaning plant surfaces. Ann. Bot. 79, 667–677 48. Breazeale, E.L. and McGeorge, W.T. (1953) Exudation pressure in roots of tomato plants under humid conditions. Soil 75, 293–298 49. Schreel, J.D.M. et al. (2019) Hydraulic redistribution of foliar absorbed water causes turgor-driven growth in mangrove seedlings. Plant Cell Environ. 42, 2437–2447 50. Lockhart, J.A. (1965) An analysis of irreversible plant cell elongation. J. Theor. Biol. 8, 264–275 51. Steppe, K. et al. (2006) A mathematical model linking tree sap flow dynamics to daily stem diameter fluctuations and radial stem growth. Tree Physiol. 26, 257–273 52. Laur, J. and Hacke, U.G. (2014) Exploring Picea glauca aquaporins in the context of needle water uptake and xylem refilling. New Phytol. 203, 388–400 53. Brodersen, C.R. et al. (2010) The dynamics of embolism repair in xylem: In vivo visualizations using high-resolution computed tomography. Plant Physiol. 154, 1088–1095 54. Vergeynst, L.L. (2015) Investigation and application of the acoustic emission technique to measure drought-induced cavitation in woody plants. 55. Brodersen, C.R. and McElrone, A.J. (2013) Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Front. Plant Sci. 4, 1–11 56. Burgess, S.S.O. and Dawson, T.E. (2007) Predicting the limits to tree height using statistical regressions of leaf traits. New Phytol. 174, 626–636 57. Gotsch, S.G. et al. (2014) Foggy days and dry nights determine crown-level water balance in a seasonal tropical montane cloud forest. Plant Cell Environ. 37, 261–272 58. Breshears, D.D. et al. (2008) Foliar absorption of intercepted rainfall improves woody plant water status most during drought. Ecology 89, 41–47 59. Binks, O. et al. (2019) Foliar water uptake in Amazonian trees: evidence and consequences. Glob. Chang. Biol. 25, 2678–2690 60. Ling, F. and Silberbush, M. (2002) Response of maize to foliar vs. soil application of nitrogen-phosphorus-potassium fertilizers. J. Plant Nutr. 25, 2333–2342 61. Bakht, J. et al. (2010) Effect of foliar vs soil application of nitrogen on yield and yield components of wheat varieties. Pakistan J. Bot. 42, 2737–2745 62. López-Arredondo, D.L. and Herrera-Estrella, L. (2012) Engineering phosphorus metabolism in plants to produce a dual fertilization and weed control system. Nat. Biotechnol. 30, 889–893

63. Wuyts, K. et al. (2015) Contributing factors in foliar uptake of dissolved inorganic nitrogen at leaf level. Sci. Total Environ. 505, 992–1002 64. Reuveni, R. and Reuveni, M. (1998) Foliar-fertilizer therapy - a concept in integrated pest management. Crop Prot. 17, 111–118 65. Adriaenssens, S. et al. (2011) Foliar nitrogen uptake from wet deposition and the relation with leaf wettability and water storage capacity. Water Air Soil Pollut. 219, 43–57 66. Bondada, B.R. et al. (2001) Urea nitrogen uptake by citrus leaves. HortScience 36, 1061–1065 67. Papini, A. et al. (2009) The ultrastructure of the development of Tillandsia (Bromeliaceae) trichome. Flora 205, 94–100 68. Peuke, A.D. et al. (1998) Foliar application of nitrate or ammonium as sole nitrogen supply in Ricinus communis II. The flows of cations, chloride and abscisic acid. New Phytol. 138, 625–636 69. Bethea, F.G. et al. (2014) Effects of acute moisture stress on creeping bentgrass cuticle morphology and associated effects on foliar nitrogen uptake. HortScience 49, 1582–1587 70. IPCC (2018) Global Warming of 1.5°C: An IPCC Special Report, IPCC 71. Ciais, P. et al. (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 72. Hauser, M. et al. (2017) Methods and model dependency of extreme event attribution: the 2015 European drought. Earth’s Futur. 5, 1034–1043 73. Lewis, S.L. et al. (2011) The 2010 Amazon drought. Science (80-. ) 331, 554 74. Allen, C.D. et al. (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6, 1–55 75. Jiménez-Muñoz, J.C. et al. (2016) Record-breaking warming and extreme drought in the Amazon rainforest during the course of El Niño 2015-2016. Sci. Rep. 6, 1–7 76. Schreel, J.D.M. et al. (2019) Influence of drought on foliar water uptake capacity of temperate tree species. Forests 10, 562 77. Gotsch, S.G. et al. (2015) Life in the treetops: ecophysiological strategies of canopy epiphytes in a tropical montane cloud forest. Ecol. Monogr. 85, 393–412 78. Eller, C.B. et al. (2016) Cloud forest trees with higher foliar water uptake capacity and anisohydric behavior are more vulnerable to drought and climate change. New Phytol. 211, 489–501 79. Bennett, A.C. et al. (2015) Larger trees suffer most during drought in forests worldwide. Nat. Plants 1, 1–5 80. McDowell, N. et al. (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought ? New Phytol. 178, 719–739 81. Ryan, M.G. (2011) Tree responses to drought. Tree Physiol. 31, 237–239 82. Anderegg, W.R.L. et al. (2012) Linking definitions, mechanisms, and modeling of drought-induced tree death. Trends Plant Sci. 17, 693–700 83. Teskey, R. et al. (2014) Responses of tree species to heat waves and extreme heat events. Plant Cell Environ. 38, 1699–1712 84. Norby, R.J. and Luo, Y. (2004) Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. New Phytol. 162, 281–293 85. Boucher, J.-F. et al. (1995) Foliar absorption of dew influences shoot water potential and root growth in Pinus strobus seedlings. Tree Physiol. 15, 819–823 86. Emery, N.C. (2016) Foliar uptake of fog in coastal California shrub species. Oecologia 182, 731–742 87. Caird, M.A. et al. (2007) Nighttime stomatal conductance and transpiration in C3 and C4 plants. Plant Physiol. 143, 4–10 88. Gouvra, E. and Grammatikopoulos, G. (2003) Beneficial effects of direct foliar water uptake on shoot water potential of five chasmophytes. Can. J. Bot. 81, 1278–1284 89. Villar-Salvador, P. et al. (2004) Drought tolerance and transplanting performance of holm oak (Quercus ilex) seedlings after drought hardening in the nursery. Tree Physiol. 24, 1147–1155

Trends in Plant Science, Month 2020, Vol. xx, No. xx

13

Trends in Plant Science

90. Stanton, K.M. and Mickelbart, M.V. (2014) Maintenance of water uptake and reduced water loss contribute to water stress tolerance of Spiraea alba Du Roi and Spiraea tomentosa L. Hortic. Res. 1, 1–7 91. Gotsch, S.G. et al. (2016) Plant carbon and water fluxes in tropical montane cloud forests. J. Trop. Ecol. 32, 404–420 92. Schreel, J.D.M. and Steppe, K. (2019) Foliar water uptake changes the world of tree hydraulics. NPJ Clim. Atmos. Sci. 2, 1 93. Earles, J.M. et al. (2019) Embracing 3D complexity in leaf carbon–water exchange. Trends Plant Sci. 24, 15–24

14

Trends in Plant Science, Month 2020, Vol. xx, No. xx

94. Stone, E.C. (1963) The ecological importance of dew. Q. Rev. Biol. 38, 328–341 95. Stone, E.C. (1957) Dew as an ecological factor: I. A review of the literature. Ecology 38, 407–413 96. Brierley, W.G. (1934) Absorption of water by the foliage of some common fruit species. Am. Soc. Hortic. Sci. 32, 277–283 97. Breazeale, E.L. et al. (1950) Moisture absorption by plants from an atmosphere of high humidity. Plant Physiol. 25, 413–419