Unravelling foliar water uptake pathways: The contribution of stomata and the cuticle

Abstract

Plants can absorb water through their leaf surfaces, a phenomenon commonly referred to as foliar water uptake (FWU). Despite the physiological importance of FWU, the pathways and mechanisms underlying the process are not well known.Using a novel experimental approach, we parsed out the contribution of the stomata and the cuticle to FWU in two species with Mediterranean (Prunus dulcis) and temperate (Pyrus communis) origin. The hydraulic parameters of FWU were derived by analysing mass and water potential changes of leaves placed in a fog chamber. Leaves were previously treated with abscisic acid to force stomata to remain closed, with fusicoccin to remain open, and with water (control). Leaves with open stomata rehydrated two times faster than leaves with closed stomata and attained approximately three times higher maximum fluxes and hydraulic conductance. Based on FWU rates, we propose that rehydration through stomata occurs primarily via diffusion of water vapour rather than in liquid form even when leaf surfaces are covered with a water film. We discuss the potential mechanisms of FWU and the significance of both stomatal and cuticular pathways for plant productivity and survival.

Foliar water uptake via cork warts in mangroves of the Sonneratia genus

“…where Ψ i and Ψ f are the initial and final leaf water potentials, respectively, C leaf is FWU divided by the absolute change in Ψ (Ψ f À Ψ i ) measured on individual leaves, and t is the duration leaf wetting (Binks et al, 2019;Brodribb & Holbrook, 2003;Guzm an-Delgado et al, 2021).…”

“…Though the value of intercepted atmospheric water sources may be greatest during drought (Breshears et al, 2008), differences between the effects of drought and leaf dehydration on FWU kinetics remain unclear. Numerous studies have reported increases in mass and leaf water potential (Ψ leaf ) with leaf wetting (Berry et al, 2019); however, leaf conductance to surface water (K surf ; μmol H 2 O s À1 m À2 MPa À1 ), which normalizes the flux into the leaf by the driving gradient, has been reported far less (Binks et al, 2016(Binks et al, , 2019Fuenzalida et al, 2019;Guzm an-Delgado et al, 2021;Guzm an-Delgado, Earles, & Zwieniecki, 2018). Among species and FWU pathways, differences in K surf and FWU rehydration kinetics with respect to seasonality and dehydration offer insights into how FWU might be integrated in plant-water movement frameworks in different ecosystems.…”

“…Intuitively, the most parsimonious FWU pathways explaining the phylogenetic ubiquity of FWU are pathways held in common, that is, stomata and/or cuticle permability (Berry et al, 2019; Fernández et al, 2017). However, while gas‐phase water uptake via stomata may explain some degree of FWU observations (Binks, Coughlin, Mencuccini, & Meir, 2020; Guzmán‐Delgado, Laca, & Zwieniecki, 2021; Vesala et al, 2017), liquid‐phase uptake of water via stomata appears to remain conditional on the reduction of hydrophobicity of guard cells via additional solutes (Burkhardt, 2010; Burkhardt, Basi, Pariyar, & Hunsche, 2012; Schönherr & Bukovac, 1972). Furthermore, while cuticle permeability to leaf surface water has also been reported in several species, valid generalizable models of FWU directly through plant cuticles remain elusive due to inconsistency among species (Fernández et al, 2017).…”

No Evidence for Light-Induced Embolism Repair in Cut Stems of Drought-Resistant Mediterranean Species under Soaking

“…Leaf trichomes, depending on their density, composition and structure, are the major media for water absorption in a Mediterranean (Quercus ilex) and a temperate (Fagus sylvatica) species [5,6]. In addition, in two species without leaf trichomes or hydathodes, open stomata have been observed to play a major role in water uptake over cuticles when exposed to fog [7]. Leaf water absorption can also be involved in the recovery of leaf [8] and stem [9,10] hydraulic functions after drought-or frost-induced xylem embolism.…”

Shoot dimorphism enables Sequoia sempervirens to separate requirements for foliar water uptake and photosynthesis

“…The pathway water takes when entering Sequoia leaves is still unknown; wax coverage and stomatal density most strongly increase hydraulic resistance, suggesting that water crosses the cuticle, yet larger stomatal size modestly lowers resistance, indicating that some water may enter that way (Figure 3A). In angiosperms, two-thirds of fog uptake enters leaves as vapor diffusing through stomata with the rest crossing the cuticle (Guzmán-Delgado et al, 2021); however, further work is needed to explore uptake pathways in conifers. Peripheral leaves with especially low visible wax coverage do not have uptake rates as high as axial shoots with comparable wax levels (Figure 3B), suggesting that other traits are influential.…”